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Infant eye and head movements toward the side opposite the cue in the anti-saccade paradigm

Infant eye and head movements toward the side opposite the cue in the anti-saccade paradigm Background: The anti-saccade task, when people must respond in the direction opposite to a visual stimulus, has been used as a marker of operation of the frontal cortical oculomotor area. However, early development of oculomotor control has been little studied with the infant anti-saccade paradigm, and a few studies did not recognize anti-saccades in infants in light of the results of adult anti-saccade. Since the characteristics of infant eye movements are little known, applying the criteria used in adult study is by no means the best way to study infant anti-saccade. As it is indicated that coordinated eye and head movements often enable infants to control the direction of their gaze, head movements should be examined as an infant orienting response. The aim of this study was to address how infants used eye and head movements during the anti-saccade paradigm. To distinguish infants' responses, we also investigated eye and head movements during a task for an inhibition of return. Inhibition of return, in which delayed responses occur in the direction to which attention had previously been oriented, has been thought to mark activity of the superior colliculus. Since the superior colliculus is thought to develop much earlier in life than the frontal lobes, we thought it useful to compare these task performances during infancy. Methods: Infants were divided into three groups according to age. Anti-saccade and inhibition-of-return tasks were given. Their eye and head movements during tasks were independently recorded by the corneal reflection method in the head-free condition. Results: Younger infants tended to initiate eye movement less than older ones in both tasks. In the anti- saccade task, responses opposite to the cue tended to show longer latency than responses to the cue. Infants made faster responses toward the side opposite the cue when it was to the right than when it was left of fixation. Regarding the comparison of responses toward the side opposite the cue between two tasks, the leftward eye movement was faster than the leftward head movements in the inhibition-of-return task, while no difference of latency was observed between eye and head movements in the anti-saccade task. A qualitative analysis of the trajectory of these responses revealed that head movement trajectories were steeper in the anti-saccade than in the inhibition-of-return task. Conclusion: Younger infants move head and eyes together, with head movements frequently starting first. On the other hand, both the leftward latency difference between eye and head and gentle trajectories of head in inhibition of return indicate that eye movements are more predominant over head movements in the inhibition-of-return task than in the anti-saccade task. This would suggest an earlier developing inhibition-of-return mechanism. Page 1 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 infants can reportedly be trained to make saccades at par- Background A crucial marker of eye movement is the ability to sup- ticular spatial locations [7,8]. press saccades toward a suddenly appearing peripheral stimulus (pro-saccade), while making a saccade in the In a few cross-sectional studies [9-11], pro- and anti-sac- opposite direction instead (anti-saccade). In an anti-sac- cades of subjects more than 5 years old have been exam- cade task, subjects are instructed not to look at a flashed ined in the general head-restrained condition to cancel cue, but to make a saccade in the opposite direction [1]. out the effects of head movements. The characteristics of That requires the willful inhibition of a strong drive to the saccades in the head-free condition may vary accord- reflexively orient one's gaze to an abrupt visual stimulus. ing to head movements. For example, a primate's saccades Using pro- and anti-saccade tasks, Munoz et al [2] occurring in a head-free condition showed slower velocity revealed that children and adults diagnosed with atten- or a depressed velocity-amplitude slope, relative to sac- tion deficit hyperactive disorders (ADHD) have great dif- cades occurring with the head fixed [12]. In order to dif- ficulties in suppressing unwanted saccades and ferentiate between head-fixed and head-free saccadic eye voluntarily controlling their fixation behavior. They movements, they have been termed eye saccades and gaze pointed to how the known fronto-striatal pathophysiol- saccades, respectively. ogy producing the symptoms of ADHD can damage the development of oculomotor control. There is a growing Meanwhile, little is known about the infant head-free sac- interest in oculomotor control in developmental disor- cadic eye movements. Infant head movements have been ders. mainly examined during visual pursuit in tracking of vis- ual stimuli in order to study development of eye-head Both Johnson [3] and Scerif et al. [4] tested infants' ability coordination [see [13]]. Johnson [3] and Scerif et al. [4] to inhibit saccades with an infant anti-saccade paradigm. investigated infant oculomotor control with no specific Infant saccades were investigated by manipulating the concern as to its relationship with head movement. spatial relationship between central and peripheral stim- Although Regal et al. [14] noted that coordinated eye and uli and the location where attractive stimuli appear. A head movements often enable infants to control the direc- similar presentation sequence (Figure 1a) was used in the tion of their gaze, no one has studied how head move- present study. Giving verbal instruction to a young infant ments are used by infants during an anti-saccade to look to the side opposite the cued side is impossible. paradigm. Instead, one must encourage them to look at the second stimulus (the target) more than the first one (the cue) by Until now we have attempted to quantify infant eye making the second stimulus more attractive than the first movements in the head-free condition, measuring eye one. After a number of such trials, Johnson [3] observed and head movements independently at the same time the decrease in responding to the cue, which predicted the [15]. In the present study, in applying our quantitative appearance of attractive stimuli at a contralateral location. method, we examine the infant look toward the second However, he concluded that 4-month-olds did not pro- stimuli (target) in the absence of response toward the first duce anti-saccades toward the target location in light of stimuli (cue) in an anti-saccade task (Figure 1a). These the results of adult anti-saccade (e.g., [5]). Scerif et al. [4] responses to the target were compared with their also did not recognize anti-saccades in infants, as they responses to the cued side. In each trial we measured both classified subjects' responses following the criteria used in eye and head latencies, respectively. In their infant study adult study [5]. Thus, previous infant studies used adult regarding the coordination of eye and head movement in criteria to classify infant responses in the anti-saccade task. order to capture peripheral visual stimuli, Regal et al. [14] pointed out that the pattern according to which infant However, saccade characteristics themselves in young head movement precedes their eye movement is not infants have been little studied systematically [6]. For found in adults. example, as a methodological issue, it is not easy to restrict head movement and calibrate each subject, both Moreover, to distinguish infants' responses toward the of which are requisite for quantitative eye movement above-mentioned non-cued side in the anti-saccade task, study. Thus, since the characteristics of infant saccades we also compared them with their responses during the were little known, applying the criteria used in adult study task for an inhibition of return. The function of inhibition was not by any means the best way to examine infant anti- of return is to bias the subject to orienting toward novel saccade. Or infant responses during the task should be objects and locations and away from previously inspected investigated before applying the criteria or being classi- ones [16]. To be specific, in a spatial cuing paradigm for fied. While neither Johnson [3] nor Scerif et al. [4] recog- inhibition of return (Figure 1b), peripheral cues facilitate nized "anti-saccade" in early infants, by 4 months of age, the processing of targets at cued locations for approxi- mately 300 ms. However, with longer latencies between Page 2 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 a) b) Fixation Fixation Cue 100 ms Cue 100 ms Delay 400 ms Fixation 900 ms Target Targets Stimu Figure 1 lus sequence used in a) task of anti-saccade and b) task of inhibition of return Stimulus sequence used in a) task of anti-saccade and b) task of inhibition of return. cue and targets, a spatial cue draws attention to that loca- dysfunction in various disease conditions [18], the early tion reflexively, inducing an inhibition of saccades toward development of responses during that task is worth stud- the cued location. In that covert method, a peripheral cue ying. Preliminarily, we also attempt to conduct a quanti- is presented so briefly that a saccade is not initiated. tative analysis of amplitude, velocity and latency of infant Therefore, inhibition of return seen from a covert para- eye and head movements, in the head-free condition, dur- digm using spatial cuing can also be called a reaction ing anti-saccade and inhibition-of-return tasks. toward the opposite side from where the cue stimulus is given. However, these responses in the inhibition-of- Methods return task are thought to be exogenously-driven auto- Subjects Twenty-nine infants, ranging in age from 3 to 11 months matic responses and to mark activity of the phylogeneti- cally ancient superior colliculus [17]. On the other hand, (mean = 7.6 months, median = 7 months), were recruited those in the anti-saccade task are thought to be endog- through local maternity groups. All gave informed con- enously controlled and to require more computational sent from their parents before the experiments. The study resources [3]. To our knowledge, no one has yet made a was approved by the Ethics Committee of Nagoya City quantitative comparison of eye and head movements dur- University (No. 2) and accorded with the ethical stand- ing anti-saccade versus inhibition-of-return tasks. We ards specified in the 1964 Declaration of Helsinki. Infants want to see if the inhibition of return shows signs of matu- were divided into three groups by age: eight 3- to 5- rity well before the anti-saccade task, since it is based on month-olds (4 male, 4 female), ten 6- to 8-month-olds (4 an older neural system which develops earlier. male, 6 female), and eleven 9- to 11-month-olds (6 male, 5 female). Criteria for admission into the study were: no The main purpose of the present study is to determine known birth defects or other kinds of complications, full how infants used eye and head movements toward the term (more than 37 weeks gestation), and normal birth side opposite the cued location, and to examine the char- weight (2500 g–4000 g). The data from another 4-month- acteristics of such movements during an anti-saccade task. old, two 5-month-olds, two 9-month-olds, and one 11- Since anti-saccade task has emerged as an important tool month-old were excluded because they were able to com- for investigating not only normal brain function, but also plete less than half of the inhibition-of-return or anti-sac- Page 3 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 cade task trials. And one 11-month-old was dropped Eye movements were recorded by the corneal reflection because he refused application of a sticking plaster to his method. To measure infant head movements, a small forehead, which is explained in the following eye move- chrome steel ball bearing (4.75 mm) was stuck to around ment section. Even if infants completed enough trials, at the middle of the subject's forehead (Figure 2) and its times, we entirely failed to track the eye or head move- reflected image was also recorded (SONY DSR-11). Beams ments by the X-Y tracker as in the following section. Thus, of invisible infrared light (LED: SLR-938C) were directed owing to the insufficiency of the contrast in video images at the subject's eye from the upper right. The reflected of infant faces, the X-Y tracker could not detect the bright- images of corneas and the chrome ball bearing were est (or darkest) portions of the CCD sensor. Therefore, the caught by a near infrared CCD camera (Hamamatsu Pho- data from one 5-month-old and two 6-month-olds were tonics, C3077-78) which was set up on the subject's lower also excluded. left (see Additional file 1). The TV signal was digitized to a two-dimensional scale by an XY-tracker unit (Hama- Each session, which consisted of inhibition-of-return and matsu Photonics, C3162) off-line. This digitizer converted anti-saccade tasks, was scheduled for approximately 30 some of the brightest (or darkest) portions of the CCD min during the infants' most alert time of day. If the infant sensor to digitized data with an absolute accuracy of 5118 was in a bad mood or not alert, the session was resched- × 3864 pixels at each 33.3 ms of sampling time. The per- uled. Upon arrival at the session room, the experimenter formance of the left eye was analyzed. explained the general procedure while a research assistant Calibration handed the infant some warm-up toys to play with. After the infant seemed adjusted to both the room and the An exact method of calibration has not yet been found. research assistant, the infant and mother were escorted to Since it is difficult to communicate verbally with infants, a semi-dark area surrounded by a blackout curtain. After they can not be expected to follow orders involved in a completing one of two tasks, the infant and mother were calibration procedure. However, we applied the experi- escorted outside of the semi-dark area and the infant was mental tentative calibration method of Koga et al. [15], soothed by the mother or the research assistant. Then they which employs the analysis of distribution of data of the were taken back into the semi-dark area for the other task. landing position for gaze and head to determine the most During the experiments, the mother, though out of sight, likely frequent landing position. This approach relied on was never far from the infant. At the end of the session, the the eye and head movements during an experiment rather mother was given the Infant Behavior Questionnaire- than in a separate calibration session. It is based on gen- Revised (IBQ-R Japanese version) and asked to complete eral assumptions about human eye and head movements and return it. in peripheral vision. Thus, since an infant's eyes and head are both initially fixed on a central point, both are in the Eye movement recording straight-ahead position (0 degree). Next, when a target is The infant sat in an experimental baby chair 65 cm away shown approximately 30 degrees right or left in the field from the color monitor of an AV tachistoscope (IS-702) in of vision, the eye is first directed to it. A head movement a semi-dark area. The experimenter outside the semi-dark follows, as a result of which the eye is positioned over the area monitored the subject's eye movements through a target. To compensate for this overshoot, the eye moves low-angle CCD near-infrared video camera (ELMO backward in relation to the head. As a result, the eye even- CN43H) set in front of the infant, and controlled the stim- tually returns to its primary position with both eye and ulus presentation on the monitor by means of a micro- head together facing the target. Besides, in some trials, computer (FMV-S167). The stimuli presented were peripheral stimulus localization was accomplished superimposed synchronously on video images of the eye almost exclusively with the eyes, while the head moved movements by a digital image processor (FOR-A, MF-310) very little. and recorded on videotape (SONY DSR-11), which was then used for off-line video coding (Figure 2). The central The calibration method of Koga et al. [15] makes the XY- fixation stimuli appeared on the color monitor, while the tracker values – the second most frequent outputs – corre- peripheral stimuli were reflected in a first-surface mirror spond to a visual angle of 30 degrees. Then, using these on the left or right side to maintain an appropriate dis- values, the so-called calibration scale factors, the XY- tance from the central fixation of approximately 30 deg. tracker outputs were linearly transformed into a visual Since head movements seldom occur in response to stim- angle. Here, it should be recalled that the result of the uli of target eccentricities of less than 20 deg [12], locali- transformation is an absolute, not a relative, value. zation at the above eccentricity (30 deg) could be accomplished with saccadic eye and head movements. Because in our research the infants can move their head freely, the eye position detected through the corneal reflection is an amalgam of the eye position in the orbit Page 4 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 Recorded Figure 2 video image of 6-month-old infant, in which the visual stimuli were superimposed Recorded video image of 6-month-old infant, in which the visual stimuli were superimposed. To measure head movements, a small chrome steel ball bearing was affixed to the forehead using a black-colored sticking plaster. and the head position in space. To obtain the eye posi- lar to those used in the anti-saccade task. As before, after tions in the orbit or relative to the head, we subtract the the key was pressed, a peripheral cue appeared to the right head position outputs (which are a reflection of the or left of the fixation stimuli. The cue, a yellow triangle (3 chrome ball on the infant's forehead) from the corneal degrees in width), was presented for 100 ms without the reflection outputs. The XY-tracker's outputs were linearly central fixation. As the cue disappeared, the central stimu- transformed into visual angles in terms of both the eye lus reappeared for 900 ms. Following offset of the central positions relative to the head and the head positions rela- stimulus, the bilateral target was presented. The target was tive to space. Then, to compute the eye position relative to composed of moving colored abstract shapes associated space (gaze) in a visual angle, the eye positions relative to with auditory signals, the two sides of which were always the head and the head positions relative to space were identical. The experiment consisted of a total of 32 trials, added. As a result of these operations, we found the point with 16 left and 16 right cues in pseudo-random order. in space where the eye gazed, and that position represents the amplitude of the gaze in a visual angle. Latencies In the present study, only the horizontal component (x- Anti-saccade task axis) was analyzed from the two-dimensional coordina- The procedure in the anti-saccade task (Figure 1a) fol- tion (horizontal and vertical outputs) produced by the X- lowed that of Johnson [3]. The centering fixation stimuli Y tracker, allowing us to examine latencies, amplitudes were composed of brightly-colored moving abstract fig- and velocity. ures and subtended 5 degrees of the visual angle. The stimuli were accompanied by synchronized sounds. We defined latency as the elapsed time between the sam- While the infant looked at the fixation, the experimenter pling time at the cue presentation and the time at the max- pressed a key, which triggered presentation of the cue, a imum acceleration for each trial of each infant. We used yellow triangle (3 degrees in width), on one of the two latencies to investigate whether a head movement pre- sides. The peripheral cue was presented for 100 ms cedes an eye movement in younger infants. together with the central fixation. Following the offset of both the central and cue stimuli, there was a 400-ms gap The maximum acceleration is obtained through a series of before presentation of the target on the side opposite that calculations. First, to ascertain the velocity (v ) of a hori- on which the cue had appeared. The target was composed zontal eye movement at the ith sampling time, we should of colored shapes moved in synchrony with simple know the gradient of the horizontal outputs (x ) at the ith sounds. The experiment consisted of a total of 32 trials, sampling time. This gradient was computed by the for- with 16 left and 16 right targets in pseudo-random order. mula (x - x )/(2/30). Here, 2/30 stands for the elapsed i+1 i-1 The training phase consisted of the first five trials, after time from the (i - 1)th sampling time to the (i + 1)th one. which the test phase of the experiment began. This operation is equivalent to the first differential of the horizontal eye movement with respect to time. Next, by Inhibition-of-return task differentiation of the derived velocity, i.e., through the The inhibition-of-return task procedure (Figure 1b) fol- equation (v - v )/(2/30), we obtain the acceleration. i+1 i-1 lowed that of Butcher et al. [19]. Each trial began with the That series of operations is equivalent to the second differ- presentation of attractive centering fixation stimuli simi- ential of the horizontal eye movement with respect to Page 5 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 time. Finally, we determine the maximal acceleration for the middle-age group, and 8.4 (SD = 3.6) for the older-age each trial of each infant, and subtract the sampling time at group. The average numbers of responses directed to the the target presentation from the one at the maximum cued location were 8.8 (SD = 3.3) for the younger-age acceleration. As the calibrated data are a linear transfor- group, 9.8 (SD = 5.5) for the middle-age group, and 7.0 mation of the raw data, it does not matter whether the (SD = 4.6) for the older-age group. In any event, for each latency is based on the calibrated data or the raw data for trial, it was difficult to obtain completely digitized data comparison of an intra-infant. We opted to compute whose sampling time was 33.3 ms all in one trial round. latency based on the raw data. Looking toward cued side vs. non-cued side in anti-saccade Results paradigm Trials for analysis The latencies of each condition are presented in Table 1 We mainly analyzed those trials in which the infant's gaze during the anti-saccade task. Average reaction times for moved directly from fixation on the target locations, i.e., each experimental condition were subjected to a four-way the side opposite the cue or the cued locations. Trials in repeated measure analysis of variance (ANOVA) with the which the gaze deviated from the direct line to those loca- following factors: side (non-cued, cued), organ (eye, tions were not included in the analysis. Only responses head), direction (leftward, rightward), and age (younger, occurring after the cue onset in the anti-saccade task and middle, older). Only the main effect of the side was mar- after the target onset in the inhibition-of-return task were ginally significant (F = 3.72, p = .08). Hence, the aver- (1,11) included. Based on the videotape in which the stimuli age latency to the target side (846.0 ms, SD = 228.8) was were superimposed on video images of the eye movement longer than the average latency to the cued side (741.5 (Figure 2), two observers not directly involved in the ms, SD = 121.8). The interaction between side and direc- experiment judged whether or not the trial was adequate tion was significant (F = 8.77, p < .05). Responses (1,11) for our analysis. The coefficient of agreement between the which were directed to the side opposite the cue occurred two coders was .88. In some trials which were judged to earlier toward the right (788.5 ms) than toward the left be adequate, we failed to digitize the eye or head move- (934.3 ms), while the latencies of the responses directed ments by the X-Y tracker and had to exclude them. to the cued location were 703.1 ms to the left and 780.6 ms to the right. For the infant anti-saccade paradigm, to separate visually triggered eye movements to the target from ones that are As a result of the ANOVA mentioned above, the main prepared based on the cue, we tentatively established one effect of the organ was not significant (F = .349). Con- (1,11) criterion, i.e., responses were excluded when both eye and sequently, we defined the latency of each trial as either a head latency were longer than 1100 ms. Namely, it is up faster latency of the eye or head and conducted a three- to 600 ms post-target onset, which was defined based on way repeated measure analysis of variance (ANOVA) with the average of each infant's mean latency of responses the following factors: side (non-cued, cued), direction toward the cued side (755.3 ms ± 146.6). Here the latency (leftward, rightward), and age (younger, middle, older). of each trial was defined as either a faster latency of the eye These data were plotted in Figure 3. The main effect of the or head. That is, 600 ms is about the average latency side was not significant (F = 1.32). However, the (1,11) minus 1 SD. Then, when either the eye or head latency interaction between side and direction was significant = 10.95, p < .01). This interaction means that was less than 1100 ms, we considered it not to be visually (F (1,11) triggered. infants made faster saccade toward the side opposite the cue to the right than to the left (F = 12.32, p < .01), (1,21) After taking the steps mentioned above, the following while there were no significant differences between the numbers of responses were analyzed for each of the age saccade to the cue to the left and to the right (F = (1,21) groups. The average numbers of responses, which were 0.636). A similar asymmetry was reported with regard to directed to the side opposite the cue in the anti-saccade the anticipatory responses of infants [20]. test phase, were 7.8 (SD = 2.4) for the younger-age group, 6.6 (SD = 4.1) for the middle-age group, and 10.5 (SD = To ascertain the tendency of early age to initiate head 6.3) for the older-age group. The average numbers of movement fast, we categorized the responses of three age responses, which were directed to the cued location in the groups both to the non-cued and cued sides into three anti-saccade training and test phases, were 9.1 (SD = 5.4) kinds according to the latencies of eye and head of each for the younger-age group, 10.6 (SD = 6.1) for the middle- response: eye-first, head-first and same time. We applied a age group, and 7.8 (SD = 4.4) for the older-age group. In log-linear model to the age (3) × side (2) × organ (3) con- the task for inhibition of return, average numbers of tingency table. As a result, the model including both an responses directed to the side opposite the cue were 13.6 (SD = 6.7) for the younger-age group, 8.0 (SD = 1.4) for age × organ interaction and an age × side one best fits the Page 6 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 Table 1: Mean latencies (SD in parentheses) of the saccades during task for anti-saccade (ms) Side Organ Direction Age (months) 3~5 6~8 9~11 Non-Cued Eye Left 1004.8 (231.2) 965.2 (176.0) 813.2 (238.4) Right 821.5 (214.3) 939.7 (179.0) 766.3 (242.6) Head Left 939.2 (137.4) 1066.3 (147.5) 817.5 (233.4) Right 834.1 (218.4) 753.2 (298.0) 616.2 (217.6) Cued Eye Left 600.4 (140.5) 703.7 (142.7) 749.7 (215.2) Right 760.2 (213.5) 805.7 (61.4) 773.7 (42.6) Head Left 623.5 (166.5) 738.4 (140.4) 803.2 (198.8) Right 794.4 (221.7) 781.8 (101.8) 767.7 (47.7) direction interaction was also significant (F = 5.01, p table ( χ = 14.15, df = 6, p = .0279; AIC = 2188.78). The (2,12) < .05). age × side interaction indicates that frequency of move- ments to the non-cued side is different from that to the As for amplitude, the issue is where the eye and/or the cued one according to the age group. The age × organ head are inclined in space. Thus, to obtain the appropriate interaction shows that the frequency of eye-first responses amplitude of the eye relative to space (gaze) and the head among the younger-age group is less than that in other age relative to space in a visual angle, calibration factors for each infant must be found through the calibration proce- groups. dure [15]. However, for some infants, we could not obtain Anti-saccade paradigm vs. inhibition-of-return paradigm: the calibration factors, because the second most frequent landing position was ambiguous. Consequently, one 6- trajectories of eye and head movements month-old, one 7-month-old, one 10-month-old and one With regard to the reaction time data of the inhibition-of- 11-month-old were excluded from analysis of amplitude return task (Table 2), ANOVA was applied with the fol- lowing factors: side (non-cued, cued), organ (eye, head), after the calibration. direction (leftward, rightward), and age (younger, middle, At each sampling time, for the eye relative to the head older). The effect of side approached significance (F = (1,12) 4.09, p = .066). Thus, the average latency to the non-cued (eye), the head relative to the space (head) and the eye rel- side (586.2 ms, SD = 81.2) was faster than the average ative to the space (gaze), we calculated the harmonic mean of all available data of the infants whose calibration latency to the cued side (660.1 ms, SD = 120.8). Based on factors were determined. Figure 4 and 5 illustrate the har- these data, we considered ourselves able to observe inhi- monic mean of the eye, the head, and the gaze move- bition of return in our subjects. The interaction between organ and direction was significant (F = 5.14, p < .05). ments during task for anti-saccade and inhibition of (1,12) return as a function of sampling times by age group, Toward the left, eye movements occurred earlier (605.8 respectively. That is, y-axis in a visual angle stands for the ms) than head movements (651.0 ms), while the latencies amplitude. These saccades of both tasks are those which of the movements directed to the right were 618.2 ms for the eye and 610.5 ms for the head. The faster leftward eye occurred in the leftward direction, opposite the cue, in the available trials. movements than head movements was specially observed in the response to the non-cued side, as the side × organ × direction interaction was marginally significant (F = In Figure 4 and 5 these movements begin around the sam- (1,12) th 3.75, p = .077). That is, regarding the response side oppo- pling time for the target presentation, i.e., the 27 sam- rd pling time for anti-saccade and the 43 for inhibition of site the cue, eye movements occurred earlier (580.5 ms) return. From these target presentation times, the ampli- than head movements (652.8 ms) toward the left, while tude of gaze, head and eye continue to increase. Then the latencies of the movements directed to the right were st 560.7 ms for the eye and 534.0 ms for the head. As for the these amplitudes appear to stabilize at around the 61 st sampling time for the anti-saccade and at about the 81 responses to the cued side, the latencies of movements sampling time for the inhibition of return. On the basis of directed to the left were 631.1 ms for the eye and 649.3 ms Figure 4 and 5, we could assume steeper head movement for the head, while these toward the right were 675.7 ms for the eye and 686.9 ms for the head. The age × organ × during the anti-saccade task compared with those evoked Page 7 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 month infants showed almost equal movements during the two tasks. 3-5 6-8 Age (months) To explore the mean speed of gaze, head and eye from the 9-11 sampling time at the target presentation to the one at the maximal amplitudes, we calculated a linear regression equation between amplitude and the sampling time and found a regression weight (or slope), which we take to represent the mean speed or velocity. In Table 5 and 6, the velocity of gaze, head and eye is calculated by age group during two tasks. In the task for anti-saccade, velocities were based on data between 27 and 60 sampling times, while for inhibition of return they were based on data between 43 and 80 sampling times. Table 5 and 6 also indicate that in the inhibition-of-return task the youngest Left Right Left Right two subjects showed smaller velocity of head movement Non-cued side Cued side compared to those in the anti-saccade task, although the head velocities of 9–11 month infants did not differ Mean latencies of each faster eye or h cu cade task Figure 3 ed and cued conditions in th ead latency, to trial, wh the ree age groups du ich w right or left side, for n ere defined as rin e g anti-sac- itheo r n- a between the two tasks. Mean latencies of each trial, which were defined as either a faster eye or head latency, to the right or left side, for non- The relationship between eye and head movements dur- cued and cued conditions in three age groups during anti-sac- cade task. ing these tasks was also discussed in light of the categori- cal data mentioned above. We categorized the responses of the three age groups to the non-cued sides during the during the task for inhibition of return in the youngest two tasks into three kinds of responses: eye-first, head-first two age groups. and same time. Then we applied a log-linear model to the age (3) × task (2: Anti-saccade vs. Inhibition of return) × In Table 3 and 4, the maximal amplitudes of gaze, head and eye are presented by age group during two tasks, organ (3) contingency table. As a result, the model includ- respectively. These amplitudes correspond to each fixed ing both an age × task interaction and an age × organ inter- amplitude after the target presentation in Figure 4 and 5, action is deemed to best fit the table ( χ = 2.46, df = 6, p although the data illustrated in Figure 4 and 5 are only for saccades occurring in the leftward direction. Hence, in the = .8727; AIC = 2184.51). The age × task interaction is st anti-saccade task, the mean amplitudes between the 61 beside the point, because it shows that each age group has th and the 90 sampling time were calculated, while the a different sample size. The age × organ interaction indi- st th mean value between the 81 and 110 sampling time cates that the frequency of eye-first responses among the were calculated for inhibition of return. Table 3 and 4 younger-age group is less than that among other groups, indicate that the youngest two subjects had smaller head and that the frequency of head-first response among the movements in the inhibition-of-return task compared low- and middle-age groups is higher than that of the with those evoked in the anti-saccade task, while 9–11 older-age group. Table 2: Mean latencies (SD in parentheses) of the saccades during task for inhibition of return (ms) Side Organ Direction Age (months) 3~5 6~8 9~11 Non-Cued Eye Left 565.1 (172.0) 635.8 (202.1) 540.7 (67.9) Right 543.1 (123.5) 600.4 (173.2) 538.8 (19.5) Head Left 552.4 (164.7) 655.1 (198.9) 750.8 (246.6) Right 611.8 (109.0) 492.5 (155.5) 497.7 (170.1) Cued Eye Left 707.3 (256.8) 563.8 (158.8) 622.2 (117.0) Right 639.7 (86.4) 683.7 (252.4) 703.6 (77.8) Head Left 720.3 (262.7) 607.4 (189.9) 620.3 (130.3) Right 661.0 (74.4) 691.5 (255.3) 708.3 (38.1) Page 8 of 14 (page number not for citation purposes) Latency (ms) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 (degree) (degree) 40 40 Cue Target Cue Target 20 20 0 a) 0 a) -20 -20 Gaze Gaze Head Head Eye Inhibition of return (Left) 3-5 months -40 -40 Eye Anti-saccade (Left) 3-5 months (from 6th trial) -60 -60 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 Sampling Time (x 1/30 s) Sampling Time (x 1/30 s) (degree) (degree) Target Cue Cue Target b) 0 b) -20 -20 Gaze Gaze Head Head Eye -40 Eye -40 Inhibition of return (Left) 6-8 months Anti-saccade (Left) 6-8 months (from 6th trial) -60 -60 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 Sampling Time (x 1/30 s) Sampling Time (x 1/30 s) (degree) (degree) Cue Target Cue Target c) c) -20 -20 Gaze Head Gaze Eye -40 Head -40 Anti-saccade (Left) 9-11 months (from 6th trial) Eye Inhibition of return (Left) 9-11 months -60 -60 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 Sampling Time (x 1/30 s) Sampling Time (x 1/30 s) Illustration ta 9 Figure 4 –11 months sk in three age gr of eye-head gaze oups: a) 3saccade –5 months, b) 6–8 months, C) s during anti-saccade Ireturn ta mon Figure 5 llustths, C) 9– ration of sk in three age gr eye- 11 months head gazoup e saccades dur s: a) 3–5 months, b) 6–8 ing inhibition-of- Illustration of eye-head gaze saccades during inhibition-of- Illustration of eye-head gaze saccades during anti-saccade task in three age groups: a) 3–5 months, b) 6–8 months, C) return task in three age groups: a) 3–5 months, b) 6–8 9–11 months. Traces of Gaze, Head and Eye are eye position months, C) 9–11 months. Traces of Gaze, Head and Eye are in space, head position in space and eye position in head, eye position in space, head position in space and eye position in head, respectively. respectively. Discussion son is made to determine whether the inhibition of return The present study sought to investigate the characteristics shows signs of maturity well before the anti-saccade task, of infant eye and head movements during an anti-saccade since the superior colliculus involved in the inhibition of task. For this purpose, first, we compared the responses return is thought to develop much earlier in life than the toward the side opposite the cue with the responses to the frontal lobes. cued location in the anti-saccade task. Second, we attempted to a quantitatively analyze infant eye and head Latencies of eye and head movements in infants movements toward the side opposite the cue during tasks In general, the present eccentricity (30 deg) was accom- for anti-saccades and inhibition of return. The compari- plished with eye and head movements. With regard to the Page 9 of 14 (page number not for citation purposes) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 Table 3: Mean maximal amplitudes (SD in parentheses) of gaze, head and eye during task for anti-saccade of sampling time from 61 to 90 (deg) Age (months) 3~5 6~8 9~11 Gaze Left 17.2 (2.4) 20.6 (5.1) 33.2 (2.7) Right -6.4 (1.1) -5.9 (1.1) -19.1 (1.6) Head Left 30.3 (3.1) 29.8 (2.3) 42.6 (3.0) Right -29.5 (2.2) -21.3 (5.7) -31.1 (1.8) Eye Left -14.2 (3.1) -26.1 (2.1) -25.5 (3.5) Right 36.6 (4.4) 16.2 (1.9) 26.5 (1.1) Positive (negative) numbers mean left (right) direction. latencies of eye and head, younger infants less often initi- responses longer than 600 ms post-target onset as visually ated eye movement. These findings are consistent with triggered responses. There are two reasons for this crite- previous infant data [6,14,21]. On the other hand, human rion: 1) The method used to measure the response time adult subjects sometimes reportedly move their head in and perform calculations in this study differed from the the direction of the target before the gaze shift begins. This conventional research approach with adult subjects, in might be a distinguishing feature of the "predictive" mode which the head of the participant is stabilized or elec- of gaze shifts [22], whereas generally head movements trooculography is applied. In head-free condition, varia- should follow saccade onset [23]. However, the present tions in latency between eye and head movements, which infant results are convincing from a phylogenetical point is dependent on target eccentricity, predictability etc., of view in that a combined eye-head movement may rep- have been shown in human [26]. How gaze control is resent an older system, which is designed to change the allocated into separate commands for eye and head move- direction of gaze, but not to foveate any particular targets, ment is still unclear [27]; and 2) Describing the response while the eye saccade could be a more recent system dynamics of infants was the key objective of the present designed to bring a visual target onto the fovea [12]. study. We thus sought to analyze reactions other than Ontogenically, eye-head gaze emerges in an early stage. those that were clearly visually triggered. As a result, the Animals, like the rabbit, who have no fovea to align with latencies of responses toward the side opposite the cue the visual target, rarely make saccades without making were marginally longer than those of responses toward head movements [24]. Also in the cat, eye and head move- the cued side, as found in previous infant [4] and adult ments are closely related, as gaze control in the cat is finer studies [1,5,10,11]. This difference in latency is possibly than in the rabbit [25]. attributable to the responses toward the cued side, being an exogenously driven response, whereas the anti-sac- Infant responses during anti-saccade task cades are endogenously controlled and require more com- In the present study of the anti-saccade task, to exclude the putational resources [3]. Hence, an infant might compute measured movements to the non-cued side of visual guid- the goal of his/her movement not from the visual trigger ance, we employed our own criterion without using the but from an internal source. This is consistent with the conventional adult criterion (i.e., for a response longer previous study that 4-month-old infants readily make than 100 ms after target presentation). Thus, we regard anticipatory saccades [20,28]. As for the asymmetry of the Table 4: Mean maximal amplitudes (SD in parentheses) of gaze, head and eye during task for inhibition of return of sampling time from 81 to 110 (deg) Age (months) 3~5 6~8 9~11 Gaze Left 16.8 (2.4) 14.0 (1.9) 28.3 (6.1) Right -6.3 (0.8) -7.5 (1.1) -27.9 (4.3) Head Left 25.6 (2.2) 19.6 (5.0) 47.4 (6.1) Right -19.5 (2.4) -19.8 (2.7) -24.3 (2.6) Eye Left -11.5 (1.4) -16.1 (2.5) -20.9 (3.0) Right 21.3 (2.1) 12.5 (3.2) 25.3 (1.4) Positive (negative) numbers mean left (right) direction. Page 10 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 Table 5: Average velocity (deg/s) of gaze, head and eye during task for anti-saccade (sampling time: 27 to 60) Age (months) 3~5 6~8 9~11 Gaze Left 18.9 18.9 26.6 Right -3.0 -0.09 -12.9 Head Left 25.6 21.6 28.2 Right -24.6 -9.3 -25.3 Eye Left -12.2 -18.4 -11.0 Right 36.5 6.7 21.9 Positive (negative) numbers mean left (right) direction anticipatory saccades of infants, our findings corre- return task. No such difference was observed between eye sponded to those of Csibra et al. [20], i.e., the response and head movements in the anti-saccade task. Since we was fast toward the right. Fischer et al. [9] and Munoz et found that younger infants tend to move their head before al. [10], investigating anti-saccade task performances their eyes, the difference between the two tasks mentioned between ages 8–70 years and 5–79 years respectively, also above could suggest the faster development of inhibition- noted the same trend in asymmetry. of-return performances, and this would confirm the idea of inhibition of return being a phylogenetically ancient To confirm that these are really anti-saccades and not sac- midbrain mechanism [17,29]. Previous study showed cades toward the target, we should include the latencies in that inhibition of return reaches near-adult levels by 6 a comparable task with no cue. And the experiment using months [30], while the number of anti-saccades increased the same condition should be applied to the same infants greatly during the toddler years [4]. except that the cue-target time interval is increased, fol- lowing Guitton et al. [5]. Scerif et al. [4] chose 700 ms for Based on Figure 4 and 5, infants in all three age groups the cue-target time interval with reference to Guitton et al. made steeper head movements in the anti-saccade task, [5], and on the basis of 800 ms (to be specific, up to 100 while in the inhibition-of-return task we observed smooth ms post-target onset) distinguished between anti-saccades head movements especially in the younger two ages. In and reactive saccades, which are stimulus driven, rather other words, infants with the younger two ages made gen- than anticipatory. Although almost half of target looks tle head movement in the inhibition-of-return task, were classified as reactive saccades in Scerif et al. [4], these although they could shift their head sharply with large may well include infant anticipatory responses. amplitude. First, we thought that it could be related to the differences in the target condition. That is, in the inhibi- Performance during anti-saccade paradigm vs. inhibition- tion-of-return task, subjects were given targets in both the of-return paradigm right and left visual fields, while in the anti-saccade task, a When we compare the responses toward the side opposite target was presented only on the side opposite from that the cue during the inhibition-of-return task with anti-sac- in which the cue had appeared. In this regard, in the study cades, one of the findings is that infants tend to move eyes of the developmental course of inhibition of return in 3- before their head towards the left in the inhibition-of- and 6-month-old babies, Clohessy et al. [30] examined Table 6: Average velocity (deg/s) of gaze, head and eye during task for inhibition of return (sampling time: 43 to 80) Age (months) 3~5 6~8 9~11 Gaze Left 9.5 9.1 22.3 Right -3.8 -3.2 -13.7 Head Left 20.6 9.9 39.4 Right -17.6 -12.5 -18.7 Eye Left -6.3 -6.9 -7.8 Right 18.0 10.5 19.6 Positive (negative) numbers mean left (right) direction Page 11 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 the effect of whether the display had only one unilateral Left/right asymmetry or bilateral target. They noted that although there are Lastly, we comment on the left/right asymmetry effects some differences of reaction and movement times observed in turning behaviors. Anti-saccades occurred between the unilateral and bilateral trials, these differ- faster towards the right than the left, while in the inhibi- ences are quite small. Movement time was defined as the tion-of-return task the infant made faster leftward eye time between the subject's initial response and the time at movements than head movements in the same direction. which he or she was fixated on the periphery. As this The observed asymmetry during the anti-saccade task movement time could be related to the gradient of move- could be compatible with the physiological rightward bias ments in Figure 5, investigators' results suggest a rather in triggering eye movements [33-35]. For example, Sheliga small effect of unilateral or bilateral target on the present et al. [33] found that the trajectory of the saccades devi- difference observed in head movement. ated contralateral to the hemifield of stimulus presenta- tion, and this deviation was larger to the right. On the Another difference of experimental conditions could be other hand, the leftward bias of eye movements observed whether there is gap before the target presentation. Thus, during the inhibition-of-return task could be related to in the anti-saccade task, the fixation and cue disappeared the right lateralized ventral frontoparietal network, which 400 ms before the appearance of the eccentric target. On might involve reorienting of attention to an unattended the other hand, in the inhibition-of-return task, the cen- location or a shift of attention from a cued location to an tral fixation was replaced by targets. In infants, gap condi- uncued one [36]. Moreover, decreased performance was tions produced the fastest saccadic latencies compared to observed only when transcranial magnetic stimulation the no-overlap and overlap conditions [8,31]. Thus far, (TMS) was applied over the right frontal eye field and only since no one has noted the gap effect on the head move- when the cue was invalid, namely, when attention had to ment, it is not worth discussing observed differences be disengaged and shifted to the opposite hemifield [37]. along this line. Here, it is speculated that TMS over this region might cause the disruption in shifting attention similar to the Next, we speculate on the difference of neural substrates way it disrupts eye movement preparation. This specula- between anti-saccade and inhibition-of-return tasks. tion and the functional asymmetry observed for interfer- Cowie & Robinson [32], using electrical stimulation of ence with shifts of attention might support the present Macaques, demonstrate that both the superior colliculus leftward bias of eye movements in the inhibition-of- and gigantocellular reticular nucleus mediate head move- return task. The reason for these evident asymmetries ments during gaze shifts. The collicular head movements remains unknown. were predominantly associated with gaze shifts, while stimulation of the medullary reticular region produced Conclusion ipsilateral head movements with no shift of gaze. It is sup- We attempted to quantitatively examine the infant's eye posed that head movement from the medullary reticular and head movements in response toward the side oppo- site plays a role in several forms of head movement, such site the cue during the anti-saccade and inhibition-of- as those which are concerned with postural reflexes, return tasks in the head-free condition. In the anti-saccade started volitionally, and/or oriented to external events. We paradigm, based on the response in accord with our crite- speculate that present head movements in the inhibition ria, the tendency was to a greater latency with a response of return might correspond to the collicular head move- to the non-cued side. Moreover, these responses were ments with the gaze shifts, since inhibition of return could faster toward the right, which is a result consistent with be strongly linked to the eye movement system of the previous studies in children and adults. superior colliculus [17,29]. On the other hand, in the anti-saccade task, the medullary reticular site contributes We confirmed that younger infants move their head and more to the head movements than in the inhibition-of- eyes together, often starting with the head in both tasks. return task. Signals which emerge from the medullary However, regarding the leftward movements during inhi- reticular region lead to fast and reproducible movements bition-of-return task, the latency of eye was smaller than of the head [32]. Hence, although the oculomotor system that of head. This kind of difference in latency was not for anti-saccade is late-maturing, unlike in the inhibition- observed between eye and head movements in the anti- of-return task, from early infancy a direct command to the saccade task. Besides, head movements of responses head is possible. Thus, it would seem surprising if an observed in the anti-saccade task looked steeper than infant of a younger age were to show sharp head move- those observed in the inhibition-of-return task. We con- ments when shifting gazes. One view is that young chil- sider that these differences between the two tasks were dren (< 8 years of age), who reportedly have difficulty in because inhibition of return is based on an old, earlier the anti-saccade task [18], might accomplish anti-saccades developing neural system. However, our discussion is more easily in company with head movements. Page 12 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 10. Munoz DP, Broughton JR, Goldring JE, Armstrong IT: Age-related quite speculative in the development phase, so further performance of human subjects on saccadic eye movement research is warranted to verify these preliminary findings. tasks. 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Thir- manuscript. teenth European Conference on Eye Movements; 2005:19. 16. Posner MI, Cohen Y: Components of visual orienting. In Atten- tion and Performance Vol. X Control of language process Edited by: Additional material Bouma H, Bouwhuis DG. Hillsdale, Erlbaum; 1984:531-556. 17. Sapir A, Soroker N, Berger A, Henik A: Inhibition of return in spa- tial attention: Direct evidence for collicular generation. Nat Additional file 1 Neurosci 1999, 2:1053-1054. Video record of 6-month infant during the anti-saccade task. Upper white 18. Munoz DP, Everling S: Look away: The anti-saccade task and the voluntary control of the eye movement. Nat Rev Neurosci dot is reflection of the small steel ball bearing representing head move- 2004, 5:218-228. ments. Bottom two dots are corneal reflections; right one represents the left 19. Butcher PR, Kalverboer AF, Geuze RH: Inhibition of return in eye. These were digitized by an X-Y tracker off-line. very young infants: a longitudinal study. 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Grosbras MH, Paus T: Transcranial magnetic stimulation of the human frontal eye field: Effects on visual perception and attention. J Cogn Neurosci 2002, 14:1109-1120. Publish with Bio Med Central and every scientist can read your work free of charge "BioMed Central will be the most significant development for disseminating the results of biomedical researc h in our lifetime." Sir Paul Nurse, Cancer Research UK Your research papers will be: available free of charge to the entire biomedical community peer reviewed and published immediately upon acceptance cited in PubMed and archived on PubMed Central yours — you keep the copyright BioMedcentral Submit your manuscript here: http://www.biomedcentral.com/info/publishing_adv.asp Page 14 of 14 (page number not for citation purposes) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral and Brain Functions Springer Journals

Infant eye and head movements toward the side opposite the cue in the anti-saccade paradigm

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Springer Journals
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Copyright © 2007 by Nakagawa and Sukigara; licensee BioMed Central Ltd.
Subject
Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
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1744-9081
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10.1186/1744-9081-3-5
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17229319
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Abstract

Background: The anti-saccade task, when people must respond in the direction opposite to a visual stimulus, has been used as a marker of operation of the frontal cortical oculomotor area. However, early development of oculomotor control has been little studied with the infant anti-saccade paradigm, and a few studies did not recognize anti-saccades in infants in light of the results of adult anti-saccade. Since the characteristics of infant eye movements are little known, applying the criteria used in adult study is by no means the best way to study infant anti-saccade. As it is indicated that coordinated eye and head movements often enable infants to control the direction of their gaze, head movements should be examined as an infant orienting response. The aim of this study was to address how infants used eye and head movements during the anti-saccade paradigm. To distinguish infants' responses, we also investigated eye and head movements during a task for an inhibition of return. Inhibition of return, in which delayed responses occur in the direction to which attention had previously been oriented, has been thought to mark activity of the superior colliculus. Since the superior colliculus is thought to develop much earlier in life than the frontal lobes, we thought it useful to compare these task performances during infancy. Methods: Infants were divided into three groups according to age. Anti-saccade and inhibition-of-return tasks were given. Their eye and head movements during tasks were independently recorded by the corneal reflection method in the head-free condition. Results: Younger infants tended to initiate eye movement less than older ones in both tasks. In the anti- saccade task, responses opposite to the cue tended to show longer latency than responses to the cue. Infants made faster responses toward the side opposite the cue when it was to the right than when it was left of fixation. Regarding the comparison of responses toward the side opposite the cue between two tasks, the leftward eye movement was faster than the leftward head movements in the inhibition-of-return task, while no difference of latency was observed between eye and head movements in the anti-saccade task. A qualitative analysis of the trajectory of these responses revealed that head movement trajectories were steeper in the anti-saccade than in the inhibition-of-return task. Conclusion: Younger infants move head and eyes together, with head movements frequently starting first. On the other hand, both the leftward latency difference between eye and head and gentle trajectories of head in inhibition of return indicate that eye movements are more predominant over head movements in the inhibition-of-return task than in the anti-saccade task. This would suggest an earlier developing inhibition-of-return mechanism. Page 1 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 infants can reportedly be trained to make saccades at par- Background A crucial marker of eye movement is the ability to sup- ticular spatial locations [7,8]. press saccades toward a suddenly appearing peripheral stimulus (pro-saccade), while making a saccade in the In a few cross-sectional studies [9-11], pro- and anti-sac- opposite direction instead (anti-saccade). In an anti-sac- cades of subjects more than 5 years old have been exam- cade task, subjects are instructed not to look at a flashed ined in the general head-restrained condition to cancel cue, but to make a saccade in the opposite direction [1]. out the effects of head movements. The characteristics of That requires the willful inhibition of a strong drive to the saccades in the head-free condition may vary accord- reflexively orient one's gaze to an abrupt visual stimulus. ing to head movements. For example, a primate's saccades Using pro- and anti-saccade tasks, Munoz et al [2] occurring in a head-free condition showed slower velocity revealed that children and adults diagnosed with atten- or a depressed velocity-amplitude slope, relative to sac- tion deficit hyperactive disorders (ADHD) have great dif- cades occurring with the head fixed [12]. In order to dif- ficulties in suppressing unwanted saccades and ferentiate between head-fixed and head-free saccadic eye voluntarily controlling their fixation behavior. They movements, they have been termed eye saccades and gaze pointed to how the known fronto-striatal pathophysiol- saccades, respectively. ogy producing the symptoms of ADHD can damage the development of oculomotor control. There is a growing Meanwhile, little is known about the infant head-free sac- interest in oculomotor control in developmental disor- cadic eye movements. Infant head movements have been ders. mainly examined during visual pursuit in tracking of vis- ual stimuli in order to study development of eye-head Both Johnson [3] and Scerif et al. [4] tested infants' ability coordination [see [13]]. Johnson [3] and Scerif et al. [4] to inhibit saccades with an infant anti-saccade paradigm. investigated infant oculomotor control with no specific Infant saccades were investigated by manipulating the concern as to its relationship with head movement. spatial relationship between central and peripheral stim- Although Regal et al. [14] noted that coordinated eye and uli and the location where attractive stimuli appear. A head movements often enable infants to control the direc- similar presentation sequence (Figure 1a) was used in the tion of their gaze, no one has studied how head move- present study. Giving verbal instruction to a young infant ments are used by infants during an anti-saccade to look to the side opposite the cued side is impossible. paradigm. Instead, one must encourage them to look at the second stimulus (the target) more than the first one (the cue) by Until now we have attempted to quantify infant eye making the second stimulus more attractive than the first movements in the head-free condition, measuring eye one. After a number of such trials, Johnson [3] observed and head movements independently at the same time the decrease in responding to the cue, which predicted the [15]. In the present study, in applying our quantitative appearance of attractive stimuli at a contralateral location. method, we examine the infant look toward the second However, he concluded that 4-month-olds did not pro- stimuli (target) in the absence of response toward the first duce anti-saccades toward the target location in light of stimuli (cue) in an anti-saccade task (Figure 1a). These the results of adult anti-saccade (e.g., [5]). Scerif et al. [4] responses to the target were compared with their also did not recognize anti-saccades in infants, as they responses to the cued side. In each trial we measured both classified subjects' responses following the criteria used in eye and head latencies, respectively. In their infant study adult study [5]. Thus, previous infant studies used adult regarding the coordination of eye and head movement in criteria to classify infant responses in the anti-saccade task. order to capture peripheral visual stimuli, Regal et al. [14] pointed out that the pattern according to which infant However, saccade characteristics themselves in young head movement precedes their eye movement is not infants have been little studied systematically [6]. For found in adults. example, as a methodological issue, it is not easy to restrict head movement and calibrate each subject, both Moreover, to distinguish infants' responses toward the of which are requisite for quantitative eye movement above-mentioned non-cued side in the anti-saccade task, study. Thus, since the characteristics of infant saccades we also compared them with their responses during the were little known, applying the criteria used in adult study task for an inhibition of return. The function of inhibition was not by any means the best way to examine infant anti- of return is to bias the subject to orienting toward novel saccade. Or infant responses during the task should be objects and locations and away from previously inspected investigated before applying the criteria or being classi- ones [16]. To be specific, in a spatial cuing paradigm for fied. While neither Johnson [3] nor Scerif et al. [4] recog- inhibition of return (Figure 1b), peripheral cues facilitate nized "anti-saccade" in early infants, by 4 months of age, the processing of targets at cued locations for approxi- mately 300 ms. However, with longer latencies between Page 2 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 a) b) Fixation Fixation Cue 100 ms Cue 100 ms Delay 400 ms Fixation 900 ms Target Targets Stimu Figure 1 lus sequence used in a) task of anti-saccade and b) task of inhibition of return Stimulus sequence used in a) task of anti-saccade and b) task of inhibition of return. cue and targets, a spatial cue draws attention to that loca- dysfunction in various disease conditions [18], the early tion reflexively, inducing an inhibition of saccades toward development of responses during that task is worth stud- the cued location. In that covert method, a peripheral cue ying. Preliminarily, we also attempt to conduct a quanti- is presented so briefly that a saccade is not initiated. tative analysis of amplitude, velocity and latency of infant Therefore, inhibition of return seen from a covert para- eye and head movements, in the head-free condition, dur- digm using spatial cuing can also be called a reaction ing anti-saccade and inhibition-of-return tasks. toward the opposite side from where the cue stimulus is given. However, these responses in the inhibition-of- Methods return task are thought to be exogenously-driven auto- Subjects Twenty-nine infants, ranging in age from 3 to 11 months matic responses and to mark activity of the phylogeneti- cally ancient superior colliculus [17]. On the other hand, (mean = 7.6 months, median = 7 months), were recruited those in the anti-saccade task are thought to be endog- through local maternity groups. All gave informed con- enously controlled and to require more computational sent from their parents before the experiments. The study resources [3]. To our knowledge, no one has yet made a was approved by the Ethics Committee of Nagoya City quantitative comparison of eye and head movements dur- University (No. 2) and accorded with the ethical stand- ing anti-saccade versus inhibition-of-return tasks. We ards specified in the 1964 Declaration of Helsinki. Infants want to see if the inhibition of return shows signs of matu- were divided into three groups by age: eight 3- to 5- rity well before the anti-saccade task, since it is based on month-olds (4 male, 4 female), ten 6- to 8-month-olds (4 an older neural system which develops earlier. male, 6 female), and eleven 9- to 11-month-olds (6 male, 5 female). Criteria for admission into the study were: no The main purpose of the present study is to determine known birth defects or other kinds of complications, full how infants used eye and head movements toward the term (more than 37 weeks gestation), and normal birth side opposite the cued location, and to examine the char- weight (2500 g–4000 g). The data from another 4-month- acteristics of such movements during an anti-saccade task. old, two 5-month-olds, two 9-month-olds, and one 11- Since anti-saccade task has emerged as an important tool month-old were excluded because they were able to com- for investigating not only normal brain function, but also plete less than half of the inhibition-of-return or anti-sac- Page 3 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 cade task trials. And one 11-month-old was dropped Eye movements were recorded by the corneal reflection because he refused application of a sticking plaster to his method. To measure infant head movements, a small forehead, which is explained in the following eye move- chrome steel ball bearing (4.75 mm) was stuck to around ment section. Even if infants completed enough trials, at the middle of the subject's forehead (Figure 2) and its times, we entirely failed to track the eye or head move- reflected image was also recorded (SONY DSR-11). Beams ments by the X-Y tracker as in the following section. Thus, of invisible infrared light (LED: SLR-938C) were directed owing to the insufficiency of the contrast in video images at the subject's eye from the upper right. The reflected of infant faces, the X-Y tracker could not detect the bright- images of corneas and the chrome ball bearing were est (or darkest) portions of the CCD sensor. Therefore, the caught by a near infrared CCD camera (Hamamatsu Pho- data from one 5-month-old and two 6-month-olds were tonics, C3077-78) which was set up on the subject's lower also excluded. left (see Additional file 1). The TV signal was digitized to a two-dimensional scale by an XY-tracker unit (Hama- Each session, which consisted of inhibition-of-return and matsu Photonics, C3162) off-line. This digitizer converted anti-saccade tasks, was scheduled for approximately 30 some of the brightest (or darkest) portions of the CCD min during the infants' most alert time of day. If the infant sensor to digitized data with an absolute accuracy of 5118 was in a bad mood or not alert, the session was resched- × 3864 pixels at each 33.3 ms of sampling time. The per- uled. Upon arrival at the session room, the experimenter formance of the left eye was analyzed. explained the general procedure while a research assistant Calibration handed the infant some warm-up toys to play with. After the infant seemed adjusted to both the room and the An exact method of calibration has not yet been found. research assistant, the infant and mother were escorted to Since it is difficult to communicate verbally with infants, a semi-dark area surrounded by a blackout curtain. After they can not be expected to follow orders involved in a completing one of two tasks, the infant and mother were calibration procedure. However, we applied the experi- escorted outside of the semi-dark area and the infant was mental tentative calibration method of Koga et al. [15], soothed by the mother or the research assistant. Then they which employs the analysis of distribution of data of the were taken back into the semi-dark area for the other task. landing position for gaze and head to determine the most During the experiments, the mother, though out of sight, likely frequent landing position. This approach relied on was never far from the infant. At the end of the session, the the eye and head movements during an experiment rather mother was given the Infant Behavior Questionnaire- than in a separate calibration session. It is based on gen- Revised (IBQ-R Japanese version) and asked to complete eral assumptions about human eye and head movements and return it. in peripheral vision. Thus, since an infant's eyes and head are both initially fixed on a central point, both are in the Eye movement recording straight-ahead position (0 degree). Next, when a target is The infant sat in an experimental baby chair 65 cm away shown approximately 30 degrees right or left in the field from the color monitor of an AV tachistoscope (IS-702) in of vision, the eye is first directed to it. A head movement a semi-dark area. The experimenter outside the semi-dark follows, as a result of which the eye is positioned over the area monitored the subject's eye movements through a target. To compensate for this overshoot, the eye moves low-angle CCD near-infrared video camera (ELMO backward in relation to the head. As a result, the eye even- CN43H) set in front of the infant, and controlled the stim- tually returns to its primary position with both eye and ulus presentation on the monitor by means of a micro- head together facing the target. Besides, in some trials, computer (FMV-S167). The stimuli presented were peripheral stimulus localization was accomplished superimposed synchronously on video images of the eye almost exclusively with the eyes, while the head moved movements by a digital image processor (FOR-A, MF-310) very little. and recorded on videotape (SONY DSR-11), which was then used for off-line video coding (Figure 2). The central The calibration method of Koga et al. [15] makes the XY- fixation stimuli appeared on the color monitor, while the tracker values – the second most frequent outputs – corre- peripheral stimuli were reflected in a first-surface mirror spond to a visual angle of 30 degrees. Then, using these on the left or right side to maintain an appropriate dis- values, the so-called calibration scale factors, the XY- tance from the central fixation of approximately 30 deg. tracker outputs were linearly transformed into a visual Since head movements seldom occur in response to stim- angle. Here, it should be recalled that the result of the uli of target eccentricities of less than 20 deg [12], locali- transformation is an absolute, not a relative, value. zation at the above eccentricity (30 deg) could be accomplished with saccadic eye and head movements. Because in our research the infants can move their head freely, the eye position detected through the corneal reflection is an amalgam of the eye position in the orbit Page 4 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 Recorded Figure 2 video image of 6-month-old infant, in which the visual stimuli were superimposed Recorded video image of 6-month-old infant, in which the visual stimuli were superimposed. To measure head movements, a small chrome steel ball bearing was affixed to the forehead using a black-colored sticking plaster. and the head position in space. To obtain the eye posi- lar to those used in the anti-saccade task. As before, after tions in the orbit or relative to the head, we subtract the the key was pressed, a peripheral cue appeared to the right head position outputs (which are a reflection of the or left of the fixation stimuli. The cue, a yellow triangle (3 chrome ball on the infant's forehead) from the corneal degrees in width), was presented for 100 ms without the reflection outputs. The XY-tracker's outputs were linearly central fixation. As the cue disappeared, the central stimu- transformed into visual angles in terms of both the eye lus reappeared for 900 ms. Following offset of the central positions relative to the head and the head positions rela- stimulus, the bilateral target was presented. The target was tive to space. Then, to compute the eye position relative to composed of moving colored abstract shapes associated space (gaze) in a visual angle, the eye positions relative to with auditory signals, the two sides of which were always the head and the head positions relative to space were identical. The experiment consisted of a total of 32 trials, added. As a result of these operations, we found the point with 16 left and 16 right cues in pseudo-random order. in space where the eye gazed, and that position represents the amplitude of the gaze in a visual angle. Latencies In the present study, only the horizontal component (x- Anti-saccade task axis) was analyzed from the two-dimensional coordina- The procedure in the anti-saccade task (Figure 1a) fol- tion (horizontal and vertical outputs) produced by the X- lowed that of Johnson [3]. The centering fixation stimuli Y tracker, allowing us to examine latencies, amplitudes were composed of brightly-colored moving abstract fig- and velocity. ures and subtended 5 degrees of the visual angle. The stimuli were accompanied by synchronized sounds. We defined latency as the elapsed time between the sam- While the infant looked at the fixation, the experimenter pling time at the cue presentation and the time at the max- pressed a key, which triggered presentation of the cue, a imum acceleration for each trial of each infant. We used yellow triangle (3 degrees in width), on one of the two latencies to investigate whether a head movement pre- sides. The peripheral cue was presented for 100 ms cedes an eye movement in younger infants. together with the central fixation. Following the offset of both the central and cue stimuli, there was a 400-ms gap The maximum acceleration is obtained through a series of before presentation of the target on the side opposite that calculations. First, to ascertain the velocity (v ) of a hori- on which the cue had appeared. The target was composed zontal eye movement at the ith sampling time, we should of colored shapes moved in synchrony with simple know the gradient of the horizontal outputs (x ) at the ith sounds. The experiment consisted of a total of 32 trials, sampling time. This gradient was computed by the for- with 16 left and 16 right targets in pseudo-random order. mula (x - x )/(2/30). Here, 2/30 stands for the elapsed i+1 i-1 The training phase consisted of the first five trials, after time from the (i - 1)th sampling time to the (i + 1)th one. which the test phase of the experiment began. This operation is equivalent to the first differential of the horizontal eye movement with respect to time. Next, by Inhibition-of-return task differentiation of the derived velocity, i.e., through the The inhibition-of-return task procedure (Figure 1b) fol- equation (v - v )/(2/30), we obtain the acceleration. i+1 i-1 lowed that of Butcher et al. [19]. Each trial began with the That series of operations is equivalent to the second differ- presentation of attractive centering fixation stimuli simi- ential of the horizontal eye movement with respect to Page 5 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 time. Finally, we determine the maximal acceleration for the middle-age group, and 8.4 (SD = 3.6) for the older-age each trial of each infant, and subtract the sampling time at group. The average numbers of responses directed to the the target presentation from the one at the maximum cued location were 8.8 (SD = 3.3) for the younger-age acceleration. As the calibrated data are a linear transfor- group, 9.8 (SD = 5.5) for the middle-age group, and 7.0 mation of the raw data, it does not matter whether the (SD = 4.6) for the older-age group. In any event, for each latency is based on the calibrated data or the raw data for trial, it was difficult to obtain completely digitized data comparison of an intra-infant. We opted to compute whose sampling time was 33.3 ms all in one trial round. latency based on the raw data. Looking toward cued side vs. non-cued side in anti-saccade Results paradigm Trials for analysis The latencies of each condition are presented in Table 1 We mainly analyzed those trials in which the infant's gaze during the anti-saccade task. Average reaction times for moved directly from fixation on the target locations, i.e., each experimental condition were subjected to a four-way the side opposite the cue or the cued locations. Trials in repeated measure analysis of variance (ANOVA) with the which the gaze deviated from the direct line to those loca- following factors: side (non-cued, cued), organ (eye, tions were not included in the analysis. Only responses head), direction (leftward, rightward), and age (younger, occurring after the cue onset in the anti-saccade task and middle, older). Only the main effect of the side was mar- after the target onset in the inhibition-of-return task were ginally significant (F = 3.72, p = .08). Hence, the aver- (1,11) included. Based on the videotape in which the stimuli age latency to the target side (846.0 ms, SD = 228.8) was were superimposed on video images of the eye movement longer than the average latency to the cued side (741.5 (Figure 2), two observers not directly involved in the ms, SD = 121.8). The interaction between side and direc- experiment judged whether or not the trial was adequate tion was significant (F = 8.77, p < .05). Responses (1,11) for our analysis. The coefficient of agreement between the which were directed to the side opposite the cue occurred two coders was .88. In some trials which were judged to earlier toward the right (788.5 ms) than toward the left be adequate, we failed to digitize the eye or head move- (934.3 ms), while the latencies of the responses directed ments by the X-Y tracker and had to exclude them. to the cued location were 703.1 ms to the left and 780.6 ms to the right. For the infant anti-saccade paradigm, to separate visually triggered eye movements to the target from ones that are As a result of the ANOVA mentioned above, the main prepared based on the cue, we tentatively established one effect of the organ was not significant (F = .349). Con- (1,11) criterion, i.e., responses were excluded when both eye and sequently, we defined the latency of each trial as either a head latency were longer than 1100 ms. Namely, it is up faster latency of the eye or head and conducted a three- to 600 ms post-target onset, which was defined based on way repeated measure analysis of variance (ANOVA) with the average of each infant's mean latency of responses the following factors: side (non-cued, cued), direction toward the cued side (755.3 ms ± 146.6). Here the latency (leftward, rightward), and age (younger, middle, older). of each trial was defined as either a faster latency of the eye These data were plotted in Figure 3. The main effect of the or head. That is, 600 ms is about the average latency side was not significant (F = 1.32). However, the (1,11) minus 1 SD. Then, when either the eye or head latency interaction between side and direction was significant = 10.95, p < .01). This interaction means that was less than 1100 ms, we considered it not to be visually (F (1,11) triggered. infants made faster saccade toward the side opposite the cue to the right than to the left (F = 12.32, p < .01), (1,21) After taking the steps mentioned above, the following while there were no significant differences between the numbers of responses were analyzed for each of the age saccade to the cue to the left and to the right (F = (1,21) groups. The average numbers of responses, which were 0.636). A similar asymmetry was reported with regard to directed to the side opposite the cue in the anti-saccade the anticipatory responses of infants [20]. test phase, were 7.8 (SD = 2.4) for the younger-age group, 6.6 (SD = 4.1) for the middle-age group, and 10.5 (SD = To ascertain the tendency of early age to initiate head 6.3) for the older-age group. The average numbers of movement fast, we categorized the responses of three age responses, which were directed to the cued location in the groups both to the non-cued and cued sides into three anti-saccade training and test phases, were 9.1 (SD = 5.4) kinds according to the latencies of eye and head of each for the younger-age group, 10.6 (SD = 6.1) for the middle- response: eye-first, head-first and same time. We applied a age group, and 7.8 (SD = 4.4) for the older-age group. In log-linear model to the age (3) × side (2) × organ (3) con- the task for inhibition of return, average numbers of tingency table. As a result, the model including both an responses directed to the side opposite the cue were 13.6 (SD = 6.7) for the younger-age group, 8.0 (SD = 1.4) for age × organ interaction and an age × side one best fits the Page 6 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 Table 1: Mean latencies (SD in parentheses) of the saccades during task for anti-saccade (ms) Side Organ Direction Age (months) 3~5 6~8 9~11 Non-Cued Eye Left 1004.8 (231.2) 965.2 (176.0) 813.2 (238.4) Right 821.5 (214.3) 939.7 (179.0) 766.3 (242.6) Head Left 939.2 (137.4) 1066.3 (147.5) 817.5 (233.4) Right 834.1 (218.4) 753.2 (298.0) 616.2 (217.6) Cued Eye Left 600.4 (140.5) 703.7 (142.7) 749.7 (215.2) Right 760.2 (213.5) 805.7 (61.4) 773.7 (42.6) Head Left 623.5 (166.5) 738.4 (140.4) 803.2 (198.8) Right 794.4 (221.7) 781.8 (101.8) 767.7 (47.7) direction interaction was also significant (F = 5.01, p table ( χ = 14.15, df = 6, p = .0279; AIC = 2188.78). The (2,12) < .05). age × side interaction indicates that frequency of move- ments to the non-cued side is different from that to the As for amplitude, the issue is where the eye and/or the cued one according to the age group. The age × organ head are inclined in space. Thus, to obtain the appropriate interaction shows that the frequency of eye-first responses amplitude of the eye relative to space (gaze) and the head among the younger-age group is less than that in other age relative to space in a visual angle, calibration factors for each infant must be found through the calibration proce- groups. dure [15]. However, for some infants, we could not obtain Anti-saccade paradigm vs. inhibition-of-return paradigm: the calibration factors, because the second most frequent landing position was ambiguous. Consequently, one 6- trajectories of eye and head movements month-old, one 7-month-old, one 10-month-old and one With regard to the reaction time data of the inhibition-of- 11-month-old were excluded from analysis of amplitude return task (Table 2), ANOVA was applied with the fol- lowing factors: side (non-cued, cued), organ (eye, head), after the calibration. direction (leftward, rightward), and age (younger, middle, At each sampling time, for the eye relative to the head older). The effect of side approached significance (F = (1,12) 4.09, p = .066). Thus, the average latency to the non-cued (eye), the head relative to the space (head) and the eye rel- side (586.2 ms, SD = 81.2) was faster than the average ative to the space (gaze), we calculated the harmonic mean of all available data of the infants whose calibration latency to the cued side (660.1 ms, SD = 120.8). Based on factors were determined. Figure 4 and 5 illustrate the har- these data, we considered ourselves able to observe inhi- monic mean of the eye, the head, and the gaze move- bition of return in our subjects. The interaction between organ and direction was significant (F = 5.14, p < .05). ments during task for anti-saccade and inhibition of (1,12) return as a function of sampling times by age group, Toward the left, eye movements occurred earlier (605.8 respectively. That is, y-axis in a visual angle stands for the ms) than head movements (651.0 ms), while the latencies amplitude. These saccades of both tasks are those which of the movements directed to the right were 618.2 ms for the eye and 610.5 ms for the head. The faster leftward eye occurred in the leftward direction, opposite the cue, in the available trials. movements than head movements was specially observed in the response to the non-cued side, as the side × organ × direction interaction was marginally significant (F = In Figure 4 and 5 these movements begin around the sam- (1,12) th 3.75, p = .077). That is, regarding the response side oppo- pling time for the target presentation, i.e., the 27 sam- rd pling time for anti-saccade and the 43 for inhibition of site the cue, eye movements occurred earlier (580.5 ms) return. From these target presentation times, the ampli- than head movements (652.8 ms) toward the left, while tude of gaze, head and eye continue to increase. Then the latencies of the movements directed to the right were st 560.7 ms for the eye and 534.0 ms for the head. As for the these amplitudes appear to stabilize at around the 61 st sampling time for the anti-saccade and at about the 81 responses to the cued side, the latencies of movements sampling time for the inhibition of return. On the basis of directed to the left were 631.1 ms for the eye and 649.3 ms Figure 4 and 5, we could assume steeper head movement for the head, while these toward the right were 675.7 ms for the eye and 686.9 ms for the head. The age × organ × during the anti-saccade task compared with those evoked Page 7 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 month infants showed almost equal movements during the two tasks. 3-5 6-8 Age (months) To explore the mean speed of gaze, head and eye from the 9-11 sampling time at the target presentation to the one at the maximal amplitudes, we calculated a linear regression equation between amplitude and the sampling time and found a regression weight (or slope), which we take to represent the mean speed or velocity. In Table 5 and 6, the velocity of gaze, head and eye is calculated by age group during two tasks. In the task for anti-saccade, velocities were based on data between 27 and 60 sampling times, while for inhibition of return they were based on data between 43 and 80 sampling times. Table 5 and 6 also indicate that in the inhibition-of-return task the youngest Left Right Left Right two subjects showed smaller velocity of head movement Non-cued side Cued side compared to those in the anti-saccade task, although the head velocities of 9–11 month infants did not differ Mean latencies of each faster eye or h cu cade task Figure 3 ed and cued conditions in th ead latency, to trial, wh the ree age groups du ich w right or left side, for n ere defined as rin e g anti-sac- itheo r n- a between the two tasks. Mean latencies of each trial, which were defined as either a faster eye or head latency, to the right or left side, for non- The relationship between eye and head movements dur- cued and cued conditions in three age groups during anti-sac- cade task. ing these tasks was also discussed in light of the categori- cal data mentioned above. We categorized the responses of the three age groups to the non-cued sides during the during the task for inhibition of return in the youngest two tasks into three kinds of responses: eye-first, head-first two age groups. and same time. Then we applied a log-linear model to the age (3) × task (2: Anti-saccade vs. Inhibition of return) × In Table 3 and 4, the maximal amplitudes of gaze, head and eye are presented by age group during two tasks, organ (3) contingency table. As a result, the model includ- respectively. These amplitudes correspond to each fixed ing both an age × task interaction and an age × organ inter- amplitude after the target presentation in Figure 4 and 5, action is deemed to best fit the table ( χ = 2.46, df = 6, p although the data illustrated in Figure 4 and 5 are only for saccades occurring in the leftward direction. Hence, in the = .8727; AIC = 2184.51). The age × task interaction is st anti-saccade task, the mean amplitudes between the 61 beside the point, because it shows that each age group has th and the 90 sampling time were calculated, while the a different sample size. The age × organ interaction indi- st th mean value between the 81 and 110 sampling time cates that the frequency of eye-first responses among the were calculated for inhibition of return. Table 3 and 4 younger-age group is less than that among other groups, indicate that the youngest two subjects had smaller head and that the frequency of head-first response among the movements in the inhibition-of-return task compared low- and middle-age groups is higher than that of the with those evoked in the anti-saccade task, while 9–11 older-age group. Table 2: Mean latencies (SD in parentheses) of the saccades during task for inhibition of return (ms) Side Organ Direction Age (months) 3~5 6~8 9~11 Non-Cued Eye Left 565.1 (172.0) 635.8 (202.1) 540.7 (67.9) Right 543.1 (123.5) 600.4 (173.2) 538.8 (19.5) Head Left 552.4 (164.7) 655.1 (198.9) 750.8 (246.6) Right 611.8 (109.0) 492.5 (155.5) 497.7 (170.1) Cued Eye Left 707.3 (256.8) 563.8 (158.8) 622.2 (117.0) Right 639.7 (86.4) 683.7 (252.4) 703.6 (77.8) Head Left 720.3 (262.7) 607.4 (189.9) 620.3 (130.3) Right 661.0 (74.4) 691.5 (255.3) 708.3 (38.1) Page 8 of 14 (page number not for citation purposes) Latency (ms) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 (degree) (degree) 40 40 Cue Target Cue Target 20 20 0 a) 0 a) -20 -20 Gaze Gaze Head Head Eye Inhibition of return (Left) 3-5 months -40 -40 Eye Anti-saccade (Left) 3-5 months (from 6th trial) -60 -60 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 Sampling Time (x 1/30 s) Sampling Time (x 1/30 s) (degree) (degree) Target Cue Cue Target b) 0 b) -20 -20 Gaze Gaze Head Head Eye -40 Eye -40 Inhibition of return (Left) 6-8 months Anti-saccade (Left) 6-8 months (from 6th trial) -60 -60 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 Sampling Time (x 1/30 s) Sampling Time (x 1/30 s) (degree) (degree) Cue Target Cue Target c) c) -20 -20 Gaze Head Gaze Eye -40 Head -40 Anti-saccade (Left) 9-11 months (from 6th trial) Eye Inhibition of return (Left) 9-11 months -60 -60 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 Sampling Time (x 1/30 s) Sampling Time (x 1/30 s) Illustration ta 9 Figure 4 –11 months sk in three age gr of eye-head gaze oups: a) 3saccade –5 months, b) 6–8 months, C) s during anti-saccade Ireturn ta mon Figure 5 llustths, C) 9– ration of sk in three age gr eye- 11 months head gazoup e saccades dur s: a) 3–5 months, b) 6–8 ing inhibition-of- Illustration of eye-head gaze saccades during inhibition-of- Illustration of eye-head gaze saccades during anti-saccade task in three age groups: a) 3–5 months, b) 6–8 months, C) return task in three age groups: a) 3–5 months, b) 6–8 9–11 months. Traces of Gaze, Head and Eye are eye position months, C) 9–11 months. Traces of Gaze, Head and Eye are in space, head position in space and eye position in head, eye position in space, head position in space and eye position in head, respectively. respectively. Discussion son is made to determine whether the inhibition of return The present study sought to investigate the characteristics shows signs of maturity well before the anti-saccade task, of infant eye and head movements during an anti-saccade since the superior colliculus involved in the inhibition of task. For this purpose, first, we compared the responses return is thought to develop much earlier in life than the toward the side opposite the cue with the responses to the frontal lobes. cued location in the anti-saccade task. Second, we attempted to a quantitatively analyze infant eye and head Latencies of eye and head movements in infants movements toward the side opposite the cue during tasks In general, the present eccentricity (30 deg) was accom- for anti-saccades and inhibition of return. The compari- plished with eye and head movements. With regard to the Page 9 of 14 (page number not for citation purposes) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Right (nasal) Left (temporal) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 Table 3: Mean maximal amplitudes (SD in parentheses) of gaze, head and eye during task for anti-saccade of sampling time from 61 to 90 (deg) Age (months) 3~5 6~8 9~11 Gaze Left 17.2 (2.4) 20.6 (5.1) 33.2 (2.7) Right -6.4 (1.1) -5.9 (1.1) -19.1 (1.6) Head Left 30.3 (3.1) 29.8 (2.3) 42.6 (3.0) Right -29.5 (2.2) -21.3 (5.7) -31.1 (1.8) Eye Left -14.2 (3.1) -26.1 (2.1) -25.5 (3.5) Right 36.6 (4.4) 16.2 (1.9) 26.5 (1.1) Positive (negative) numbers mean left (right) direction. latencies of eye and head, younger infants less often initi- responses longer than 600 ms post-target onset as visually ated eye movement. These findings are consistent with triggered responses. There are two reasons for this crite- previous infant data [6,14,21]. On the other hand, human rion: 1) The method used to measure the response time adult subjects sometimes reportedly move their head in and perform calculations in this study differed from the the direction of the target before the gaze shift begins. This conventional research approach with adult subjects, in might be a distinguishing feature of the "predictive" mode which the head of the participant is stabilized or elec- of gaze shifts [22], whereas generally head movements trooculography is applied. In head-free condition, varia- should follow saccade onset [23]. However, the present tions in latency between eye and head movements, which infant results are convincing from a phylogenetical point is dependent on target eccentricity, predictability etc., of view in that a combined eye-head movement may rep- have been shown in human [26]. How gaze control is resent an older system, which is designed to change the allocated into separate commands for eye and head move- direction of gaze, but not to foveate any particular targets, ment is still unclear [27]; and 2) Describing the response while the eye saccade could be a more recent system dynamics of infants was the key objective of the present designed to bring a visual target onto the fovea [12]. study. We thus sought to analyze reactions other than Ontogenically, eye-head gaze emerges in an early stage. those that were clearly visually triggered. As a result, the Animals, like the rabbit, who have no fovea to align with latencies of responses toward the side opposite the cue the visual target, rarely make saccades without making were marginally longer than those of responses toward head movements [24]. Also in the cat, eye and head move- the cued side, as found in previous infant [4] and adult ments are closely related, as gaze control in the cat is finer studies [1,5,10,11]. This difference in latency is possibly than in the rabbit [25]. attributable to the responses toward the cued side, being an exogenously driven response, whereas the anti-sac- Infant responses during anti-saccade task cades are endogenously controlled and require more com- In the present study of the anti-saccade task, to exclude the putational resources [3]. Hence, an infant might compute measured movements to the non-cued side of visual guid- the goal of his/her movement not from the visual trigger ance, we employed our own criterion without using the but from an internal source. This is consistent with the conventional adult criterion (i.e., for a response longer previous study that 4-month-old infants readily make than 100 ms after target presentation). Thus, we regard anticipatory saccades [20,28]. As for the asymmetry of the Table 4: Mean maximal amplitudes (SD in parentheses) of gaze, head and eye during task for inhibition of return of sampling time from 81 to 110 (deg) Age (months) 3~5 6~8 9~11 Gaze Left 16.8 (2.4) 14.0 (1.9) 28.3 (6.1) Right -6.3 (0.8) -7.5 (1.1) -27.9 (4.3) Head Left 25.6 (2.2) 19.6 (5.0) 47.4 (6.1) Right -19.5 (2.4) -19.8 (2.7) -24.3 (2.6) Eye Left -11.5 (1.4) -16.1 (2.5) -20.9 (3.0) Right 21.3 (2.1) 12.5 (3.2) 25.3 (1.4) Positive (negative) numbers mean left (right) direction. Page 10 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 Table 5: Average velocity (deg/s) of gaze, head and eye during task for anti-saccade (sampling time: 27 to 60) Age (months) 3~5 6~8 9~11 Gaze Left 18.9 18.9 26.6 Right -3.0 -0.09 -12.9 Head Left 25.6 21.6 28.2 Right -24.6 -9.3 -25.3 Eye Left -12.2 -18.4 -11.0 Right 36.5 6.7 21.9 Positive (negative) numbers mean left (right) direction anticipatory saccades of infants, our findings corre- return task. No such difference was observed between eye sponded to those of Csibra et al. [20], i.e., the response and head movements in the anti-saccade task. Since we was fast toward the right. Fischer et al. [9] and Munoz et found that younger infants tend to move their head before al. [10], investigating anti-saccade task performances their eyes, the difference between the two tasks mentioned between ages 8–70 years and 5–79 years respectively, also above could suggest the faster development of inhibition- noted the same trend in asymmetry. of-return performances, and this would confirm the idea of inhibition of return being a phylogenetically ancient To confirm that these are really anti-saccades and not sac- midbrain mechanism [17,29]. Previous study showed cades toward the target, we should include the latencies in that inhibition of return reaches near-adult levels by 6 a comparable task with no cue. And the experiment using months [30], while the number of anti-saccades increased the same condition should be applied to the same infants greatly during the toddler years [4]. except that the cue-target time interval is increased, fol- lowing Guitton et al. [5]. Scerif et al. [4] chose 700 ms for Based on Figure 4 and 5, infants in all three age groups the cue-target time interval with reference to Guitton et al. made steeper head movements in the anti-saccade task, [5], and on the basis of 800 ms (to be specific, up to 100 while in the inhibition-of-return task we observed smooth ms post-target onset) distinguished between anti-saccades head movements especially in the younger two ages. In and reactive saccades, which are stimulus driven, rather other words, infants with the younger two ages made gen- than anticipatory. Although almost half of target looks tle head movement in the inhibition-of-return task, were classified as reactive saccades in Scerif et al. [4], these although they could shift their head sharply with large may well include infant anticipatory responses. amplitude. First, we thought that it could be related to the differences in the target condition. That is, in the inhibi- Performance during anti-saccade paradigm vs. inhibition- tion-of-return task, subjects were given targets in both the of-return paradigm right and left visual fields, while in the anti-saccade task, a When we compare the responses toward the side opposite target was presented only on the side opposite from that the cue during the inhibition-of-return task with anti-sac- in which the cue had appeared. In this regard, in the study cades, one of the findings is that infants tend to move eyes of the developmental course of inhibition of return in 3- before their head towards the left in the inhibition-of- and 6-month-old babies, Clohessy et al. [30] examined Table 6: Average velocity (deg/s) of gaze, head and eye during task for inhibition of return (sampling time: 43 to 80) Age (months) 3~5 6~8 9~11 Gaze Left 9.5 9.1 22.3 Right -3.8 -3.2 -13.7 Head Left 20.6 9.9 39.4 Right -17.6 -12.5 -18.7 Eye Left -6.3 -6.9 -7.8 Right 18.0 10.5 19.6 Positive (negative) numbers mean left (right) direction Page 11 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 the effect of whether the display had only one unilateral Left/right asymmetry or bilateral target. They noted that although there are Lastly, we comment on the left/right asymmetry effects some differences of reaction and movement times observed in turning behaviors. Anti-saccades occurred between the unilateral and bilateral trials, these differ- faster towards the right than the left, while in the inhibi- ences are quite small. Movement time was defined as the tion-of-return task the infant made faster leftward eye time between the subject's initial response and the time at movements than head movements in the same direction. which he or she was fixated on the periphery. As this The observed asymmetry during the anti-saccade task movement time could be related to the gradient of move- could be compatible with the physiological rightward bias ments in Figure 5, investigators' results suggest a rather in triggering eye movements [33-35]. For example, Sheliga small effect of unilateral or bilateral target on the present et al. [33] found that the trajectory of the saccades devi- difference observed in head movement. ated contralateral to the hemifield of stimulus presenta- tion, and this deviation was larger to the right. On the Another difference of experimental conditions could be other hand, the leftward bias of eye movements observed whether there is gap before the target presentation. Thus, during the inhibition-of-return task could be related to in the anti-saccade task, the fixation and cue disappeared the right lateralized ventral frontoparietal network, which 400 ms before the appearance of the eccentric target. On might involve reorienting of attention to an unattended the other hand, in the inhibition-of-return task, the cen- location or a shift of attention from a cued location to an tral fixation was replaced by targets. In infants, gap condi- uncued one [36]. Moreover, decreased performance was tions produced the fastest saccadic latencies compared to observed only when transcranial magnetic stimulation the no-overlap and overlap conditions [8,31]. Thus far, (TMS) was applied over the right frontal eye field and only since no one has noted the gap effect on the head move- when the cue was invalid, namely, when attention had to ment, it is not worth discussing observed differences be disengaged and shifted to the opposite hemifield [37]. along this line. Here, it is speculated that TMS over this region might cause the disruption in shifting attention similar to the Next, we speculate on the difference of neural substrates way it disrupts eye movement preparation. This specula- between anti-saccade and inhibition-of-return tasks. tion and the functional asymmetry observed for interfer- Cowie & Robinson [32], using electrical stimulation of ence with shifts of attention might support the present Macaques, demonstrate that both the superior colliculus leftward bias of eye movements in the inhibition-of- and gigantocellular reticular nucleus mediate head move- return task. The reason for these evident asymmetries ments during gaze shifts. The collicular head movements remains unknown. were predominantly associated with gaze shifts, while stimulation of the medullary reticular region produced Conclusion ipsilateral head movements with no shift of gaze. It is sup- We attempted to quantitatively examine the infant's eye posed that head movement from the medullary reticular and head movements in response toward the side oppo- site plays a role in several forms of head movement, such site the cue during the anti-saccade and inhibition-of- as those which are concerned with postural reflexes, return tasks in the head-free condition. In the anti-saccade started volitionally, and/or oriented to external events. We paradigm, based on the response in accord with our crite- speculate that present head movements in the inhibition ria, the tendency was to a greater latency with a response of return might correspond to the collicular head move- to the non-cued side. Moreover, these responses were ments with the gaze shifts, since inhibition of return could faster toward the right, which is a result consistent with be strongly linked to the eye movement system of the previous studies in children and adults. superior colliculus [17,29]. On the other hand, in the anti-saccade task, the medullary reticular site contributes We confirmed that younger infants move their head and more to the head movements than in the inhibition-of- eyes together, often starting with the head in both tasks. return task. Signals which emerge from the medullary However, regarding the leftward movements during inhi- reticular region lead to fast and reproducible movements bition-of-return task, the latency of eye was smaller than of the head [32]. Hence, although the oculomotor system that of head. This kind of difference in latency was not for anti-saccade is late-maturing, unlike in the inhibition- observed between eye and head movements in the anti- of-return task, from early infancy a direct command to the saccade task. Besides, head movements of responses head is possible. Thus, it would seem surprising if an observed in the anti-saccade task looked steeper than infant of a younger age were to show sharp head move- those observed in the inhibition-of-return task. We con- ments when shifting gazes. One view is that young chil- sider that these differences between the two tasks were dren (< 8 years of age), who reportedly have difficulty in because inhibition of return is based on an old, earlier the anti-saccade task [18], might accomplish anti-saccades developing neural system. However, our discussion is more easily in company with head movements. Page 12 of 14 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:5 http://www.behavioralandbrainfunctions.com/content/3/1/5 10. Munoz DP, Broughton JR, Goldring JE, Armstrong IT: Age-related quite speculative in the development phase, so further performance of human subjects on saccadic eye movement research is warranted to verify these preliminary findings. tasks. 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Grosbras MH, Paus T: Transcranial magnetic stimulation of the human frontal eye field: Effects on visual perception and attention. J Cogn Neurosci 2002, 14:1109-1120. Publish with Bio Med Central and every scientist can read your work free of charge "BioMed Central will be the most significant development for disseminating the results of biomedical researc h in our lifetime." Sir Paul Nurse, Cancer Research UK Your research papers will be: available free of charge to the entire biomedical community peer reviewed and published immediately upon acceptance cited in PubMed and archived on PubMed Central yours — you keep the copyright BioMedcentral Submit your manuscript here: http://www.biomedcentral.com/info/publishing_adv.asp Page 14 of 14 (page number not for citation purposes)

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