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Stimulus-dependent effects on tactile spatial acuity

Stimulus-dependent effects on tactile spatial acuity Background: Previous studies have shown that spatio-tactile acuity is influenced by the clarity of the cortical response in primary somatosensory cortex (SI). Stimulus characteristics such as frequency, amplitude, and location of tactile stimuli presented to the skin have been shown to have a significant effect on the response in SI. The present study observes the effect of changing stimulus parameters of 25 Hz sinusoidal vertical skin displacement stimulation ("flutter") on a human subject's ability to discriminate between two adjacent or near-adjacent skin sites. Based on results obtained from recent neurophysiological studies of the SI response to different conditions of vibrotactile stimulation, we predicted that the addition of 200 Hz vibration to the same site that a two-point flutter stimulus was delivered on the skin would improve a subject's spatio-tactile acuity over that measured with flutter alone. Additionally, similar neurophysiological studies predict that the presence of either a 25 Hz flutter or 200 Hz vibration stimulus on the unattended hand (on the opposite side of the body from the site of two-point limen testing – the condition of bilateral stimulation – which has been shown to evoke less SI cortical activity than the contralateral-only stimulus condition) would decrease a subject's ability to discriminate between two points on the skin. Results: A Bekesy tracking method was employed to track a subject's ability to discriminate between two-point stimuli delivered to the skin. The distance between the two points of stimulation was varied on a trial-by-trial basis, and several different stimulus conditions were examined: (1) The "control" condition, in which 25 Hz flutter stimuli were delivered simultaneously to the two points on the skin of the attended hand, (2) the "complex" condition, in which a combination of 25 Hz flutter and 200 Hz vibration stimuli were delivered to the two points on the attended hand, and (3) a "bilateral" condition, in which 25 Hz flutter was delivered to the two points on the attended hand and a second stimulus (either flutter or vibration) was delivered to the unattended hand. The two-point limen was reduced (i.e., spatial acuity was improved) under the complex stimulus condition when compared to the control stimulus condition. Specifically, whereas adding vibration to the unilateral two-point flutter stimulus improved spatial acuity by 20 to 25%, the two-point limen was not significantly affected by substantial changes in stimulus amplitude (between 100 – 200 µm). In contrast, simultaneous stimulation of the unattended hand (contralateral to the attended site), impaired spatial acuity by 20% with flutter stimulation and by 30% with vibration stimulation. Conclusion: It was found that the addition of 200 Hz vibration to a two-point 25 Hz flutter stimulus significantly improved a subject's ability to discriminate between two points on the skin. Since previous studies showed that 200 Hz vibration preferentially evokes activity in cortical area SII and reduces or inhibits the spatial extent of activity in SI in the same hemisphere, the findings in this paper raise the possibility that although SI activity plays a major role in two-point discrimination on the skin, influences relayed to SI from SII in the same hemisphere may contribute importantly to SI's ability to differentially respond to stimuli applied to closely spaced skin points on the same side of the body midline. Page 1 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 have been found in the non-human primate (unpub- Introduction Recently, we reported the development of a semi-auto- lished observations). This led us to the prediction that, mated method for measuring a human subject's ability to because of the decrease in prominence of the two peaks of discriminate between two points on the skin [1]. In that neuronal activity in SI evoked and consequently, the study, a Two-Point Stimulator (TPS) was employed to reduction in the spatial clarity between those peaks of cor- deliver tactile stimuli simultaneously to two separate skin tical activity, a subject's two-point limen would increase sites. Since distance between the two points of the TPS can (indicating reduced spatial acuity) with the addition of a be adjusted on a trial-by-trial basis, it was possible to stimulus to the unattended hand. employ a Bekesy tracking method to determine a subject's two-point limen under several different conditions of Results two-point stimulation. Two-point stimuli were presented Bekesy tracking algorithms were used to find a subject's to the skin under static conditions (two probes simply two-point limen at the dorsal surface of the right hand pressed into the skin), in the presence of flutter stimula- under four different stimulus conditions. Exemplary tion (probes oscillated at 25 Hz as they were pressed into results for a single session (four runs) of a subject are the skin), or in the presence of vibration (probes oscil- shown in Figure 1. The two-point limen of the subject was lated at 200 Hz). The results duplicated the finding of tracked for two points delivered simultaneously and oscil- Vierck and Jones [2] that demonstrated that oscillating the lated at 25 Hz on the attended hand (AH). The data pre- two probes improved a subject's spatial acuity (as meas- sented indicate that under this condition the subject was ured by the two-point limen). Furthermore, both our able to detect the presence of two points at a separation of study and the Vierck and Jones report showed that spatial approximately 19 mm (average response for the last five acuity is better in the 25 Hz stimulus condition than in the trials). In a second run (the "complex" stimulus condi- 200 Hz stimulus condition. tion), the two-point limen was tracked under identical conditions as the first run, with the exception that the 25 Mountcastle and Darian-Smith [3] proposed that a sub- Hz stimulus waveform was delivered with an additional ject's ability to spatially discriminate between two points 200 Hz vibration on the attended hand (see Methods). on the skin would be dependent on the lateral inhibition The addition of the 200 Hz vibration to the 25 Hz flutter that enables the formation of the peaks of neuronal activ- resulted in a decrease in the two-point limen to approxi- ity in SI cortex. Additionally, LaMotte and Mountcastle mately 16.4 mm. In the two other conditions, the two- [4,5] asserted that the capacity of a subject to accurately point limen was tracked to a two-point 25 Hz flutter stim- localize a flutter stimulus on the skin is determined by the ulus on the attended hand, under identical conditions as locus and clarity of the flutter-evoked neuron population the first run, but with the addition of a simultaneous 25 response within the topographically organized SI net- Hz flutter or 200 Hz vibration stimulus to the opposite, work. If this is the case, then the ability of a subject to dis- unattended hand (UH). Interestingly, in both cases, stim- criminate between two points would improve if the locus ulation of the unattended hand impaired the subjects' of the responses in SI to the stimuli at the two correspond- ability to discriminate between two points on the ing skin sites were more clearly defined – i.e., if the spatial attended hand, and thus, the two-point limen actually extent of the response in SI to a point stimulus waslimited increased to values of approximately 22 mm and 24 mm or reduced. Observations by Tommerdahl and colleagues for 25 Hz and 200 Hz unattended conditions, respec- demonstrated that the SI response to a complex stimulus tively. To summarize, the detection of two points pre- (one comprised of both flutter and vibration) is spatially sented simultaneously with flutter was improved with constrained when compared to the response to flutter same-site vibration and degraded with the addition of alone [6-9]. In other words, the SI response evoked by a either a flutter or vibration stimulus on the opposite, complex stimulus is smaller in spatial extent than that unattended hand. evoked by 25 Hz flutter alone. Thus, based on the effect that same-site vibration has on the SI response to flutter, To determine subject consistency of the above findings, we were led to the prediction that vibration, if presented the tracking data collected under each condition for an simultaneously at the same sites as two-point flutter stim- individual subject were averaged. The data were normal- uli (i.e., as a complex stimulus comprised of 25 Hz and ized to the flutter condition since the primary objective of 200 Hz components), would improve a subject's ability to this study was to determine the effect of vibration on the discriminate between two points. Alternatively, recent response normally evoked by two-point flutter stimula- findings comparing the SI activity evoked by different tion. Thus, the two-point limen for the flutter condition conditions of contralateral, ipsilateral and bilateral stimu- was defined as the value "1" and all other distances are lation in the cat show that the magnitude of response in plotted as a proportion of the values obtained under the SI evoked by contralateral stimulation is reduced in the flutter condition [1]. The normalized average two-point presence of an ipsilateral stimulus [10]. Similar results limen plot for one subject is displayed in Figure 2. Note Page 2 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 A Figure 1 tracking protocol was used to conduct a two-point limen threshold test A tracking protocol was used to conduct a two-point limen threshold test. Separation between the two probe tips on the attended hand (AH) versus time was observed under four conditions of stimulation. One condition consisted of 25 Hz flutter applied by the TPS on the AH. In a second condition, the two tips were applied to the AH by a complex stimulus (25 Hz+200 Hz). For the other two conditions, 25 Hz flutter was applied to the AH with either a 25 Hz flutter or 200 Hz vibration stimulus applied simultaneously to the unattended hand (UH). A single trial consisted of stimuli presented to the skin for 1 sec, and then completely removed from the skin for an inter-stimulus interval of 2 sec. Each run consisted of 30 trials, or a duration of 90 sec total. that the two-point limen was reduced (i.e., spatial acuity two-point limen values that were approximately 30% was improved) for the complex condition – the two-point higher than the control condition. limen tracks at approximately 80% of the values measured under the flutter condition. In contrast, the two-point To determine the across-subject consistency of the above limen was larger (i.e., spatial acuity is worse) for both findings, the data normalization process applied to the bilateral conditions. In the case in which the opposite or single subject case, as shown in Figure 2 and described unattended hand was presented with a simultaneous 25 above, was repeated for data collected under each condi- Hz flutter stimulus, the two-point limen tracks approxi- tion across all subjects. Normalized and averaged data are mately 20% higher than the control (attended hand only) shown in Figure 3. Similar to the data presented in Figure condition. Similarly, applying a 200 Hz vibration stimu- 2, the two-point limen for the complex condition tracked lus simultaneously to the unattended hand resulted in between 75 and 80% of that measured under the flutter Page 3 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 Figure 2 Average of two-point limen tracking, under all conditions, for one exemplary subject Average of two-point limen tracking, under all conditions, for one exemplary subject. All distances are normalized to the two- point distance recorded under the attended hand (AH) 25 Hz flutter condition. Standard error bars demonstrate that across- session variability for the two-point limen tracking method is fairly consistent. condition, indicating a 20–25% improvement in spatial dition, or when vibration was presented with flutter, by acuity resulting from the presence of vibration during the dual-site stimuli on the attended hand. Alternatively, the flutter stimulus driving the TPS on the attended hand. two-point limen increased when a second, simultaneous Alternatively, tracking of the two-point limen showed an stimulus was added to the unattended hand – approxi- increase of approximately 20% and 30% for the condi- mately 20% for the 25 Hz flutter condition and 30% for tions in which the unattended hand was stimulated with 200 Hz vibration condition. Standard error bars demon- flutter and vibration, respectively. strate that across-subject variability for the two-point limen tracking method is fairly consistent. ANOVA testing In order to more directly compare the responses measured was conducted on this data with the null hypothesis that under each of the stimulus conditions, the tracking values the mean under the control flutter condition is signifi- obtained from the last five trials across all subjects was cantly different than the means obtained under the three averaged and normalized to the flutter condition (Figure test conditions. The means for the bilateral conditions of 4). Again, it is apparent that the two-point limen values unattended hand 25 Hz (F = 47.7; p < 0.00000001) and decreased by approximately 20% under the complex con- unattended hand 200 Hz (F = 76.3; p < 0.00000001), as Page 4 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 A Figure 3 verage of two-point limen tracking across all subjects Average of two-point limen tracking across all subjects. All distances are normalized to the two-point distance recorded under the attended hand (AH) 25 Hz flutter condition. Standard error bars demonstrate that across-subject variability for the two- point limen tracking method is fairly consistent. well as the complex condition (F = 27.6; p < 0.00001) are ner as the previous results (see Figure 5). In both the 150 significantly different from the mean under the flutter and 200 µm conditions, the two-point limen oscillated condition. approximately within 10% of that observed at the 100 µm condition, suggesting that there was no consistent effect To ensure that the enhanced acuity of a subject under the on the two-point limen due to the increased amplitude of complex stimulus condition was not due simply to the the complex stimulus and that the effect seen under the increased amplitude that resulted from adding vibration complex condition was most likely attributable to the to a flutter stimulus (which resulted in a stimulus ampli- additional high-frequency component. tude of 120 µm), the two-point limen was tracked on the attended hand at 25 Hz flutter of varying amplitudes. Spe- Discussion cifically, a separate series of sessions were conducted to In the present study, we observed stimulus-dependent track and compare the two-point limen for the amplitudes effects on two-point tracking of a flutter stimulus at the of 100, 150, and 200 µm in the flutter-only condition. The dorsal surface of the attended hand. The two-point limen results were normalized to the distances observed under was reduced (spatial acuity was improved) with a complex the 100 µm condition and were plotted in the same man- stimulus that consisted of 25 Hz flutter and 200 Hz Page 5 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 A Figure 4 verage of last five trials of two-point limen tracking across all subjects, with standard error bars Average of last five trials of two-point limen tracking across all subjects, with standard error bars. All distances are normalized to the two-point distance recorded under the attended hand (AH) flutter condition. vibration components. Specifically, it was found that add- within the amplitude range used, there were no significant ing vibration to the unilateral two-point flutter stimulus differences in the two-point limen. This is also consistent improved spatial acuity by 20 to 25%. When the amplitude with the idea that increasing amplitude of a stimulus does of the unilateral two-point flutter stimulus was signifi- not increase the spatial extent of its cortical response – a cantly varied (between 100 – 200 µm), the two-point finding recently reported [12]. In that report, observations limen was not affected. Simultaneous stimulation of the obtained from imaging the optical intrinsic signal in non- hand contralateral to the attended site, however, impaired human primates showed that higher amplitudes of stimu- or reduced spatial acuity by 20% with a flutter stimulus and lation with a 25 Hz flutter stimulus in the amplitude range 30% with a vibratory stimulus. studied (50–400 µm at a frequency of 25 Hz) did not pro- duce larger areas of cortical activation in primary somato- Vega-Bermudez and Johnson [11], using grating orienta- sensory cortex (SI). Rather, the spatial extent of the tion studies, cited the importance of skin deformation as cortical patterns of activation evoked by the flutter stimu- a factor affecting spatial acuity. For this reason, we consid- lus was limited. Simons et al. postulated that the cortical ered the possibility that enhanced spatial acuity with a response is sculpted or refined by lateral inhibition, complex stimulus may be due to the fact that adding thereby limiting changes in spatial extent [12]. These find- vibration to the flutter stimulus introduces another ampli- ings are consistent with the idea that the spatial extent of tude component, thereby increasing the overall magni- the SI response evoked by each of the point stimuli plays tude of the stimulus. Results from our study showed that, a role in a subject's ability to discriminate between two Page 6 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 A a Figure 5 tten verage of two- ded hand atpoint limen tracking acr amplitudes of 100 µm, 150 oss all subjects for cont µm, or 200 µm rol conditions: 25 Hz flutter stimulus applied by the TPS to the Average of two-point limen tracking across all subjects for control conditions: 25 Hz flutter stimulus applied by the TPS to the attended hand at amplitudes of 100 µm, 150 µm, or 200 µm. All distances are normalized to the two-point distance recorded under the 25 Hz-100 µm condition. stimulus sites on the skin, since changing the amplitude of However, Summers and Chanter also stated that this type a flutter stimulus has little effect on either the spatial of interpretation (that the addition of high-frequency extent of the SI response in primates or on the two-point vibration to a lower-frequency stimulus results in limen observations made in this report. improvement in perception of that stimulus) was prob- lematic because of the known differences between mech- Summers and Chanter [13] reported results on tactile acu- anoreceptors [13]. Previous studies had established the ity in the fingertip in response to stimuli presented by a fact that spatial acuity was worse at high frequencies (in broadband tactile array. They found that localization of a the Pacinian range) than at low frequencies (RA/SA range) 40 Hz target stimulus was improved with the addition of [1,2,14]. However, if spatial acuity can be attributed to the a 320 Hz background stimulus (which surrounded the tar- spatial clarity between regions of cortical activity as get) compared to that with a 40 Hz background stimulus. LaMotte and Mountcastle [4] proposed, then the cortico- Page 7 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 cortical interactions that result from the condition of A recent report described that the ability to localize a stim- simultaneous flutter and vibration [8] would ulus on the fingertips of one hand may be impaired with undoubtedly have an effect on measures of spatial acuity. the interference of a similar stimulus on a fingertip of the Flutter stimuli, such as the ones presented in this study, opposite hand [19], suggesting that spatial acuity may be are known to evoke significant and sustained activity in SI worse with bilateral stimulation than with unilateral stim- cortex. Skin stimulation at 200 Hz, on the other hand, has ulation under certain conditions. In a separate study, we been shown to reduce the spatial extent of SI response reported that the SI cortical response to contralateral skin normally evoked by a 25 Hz flutter stimulus [6-9]. stimulation was reduced when an identical stimulus was presented simultaneously to the ipsilateral (mirror image) Tommerdahl et al. [6] compared the intrinsic signal skin site [10]. Specifically, Tommerdahl and colleagues evoked in areas 3b/1 by 25 Hz skin stimulation to the found that the magnitude of response in SI to bilateral intrinsic signal evoked by a same-site skin stimulus stimulation was 30–35% smaller than the response containing both 25 and 200 Hz sinusoidal components (a evoked by a contralateral flutter stimulus. This finding led "complex waveform stimulus"). Such experiments us to postulate that, since contralateral SI is recognized as revealed that the increase in absorbance evoked in areas the cortical region most responsible for spatial localiza- 3b/1 by a stimulus having both 25 and 200 Hz compo- tion [4,5], a reduction in the magnitude of the contralat- nents was substantially smaller than the increase in eral SI response – via ipsilateral stimulation – could cause absorbance evoked by "pure" 25 Hz stimulation of the a reduction in spatial acuity. Results from the present same skin site. It was concluded that within a brief time study support this hypothesis, suggesting that bilateral after stimulus onset, 200 Hz skin stimulation evokes a stimulation of two homologous body parts leads to a powerful inhibitory action on area 3b/1 QA neurons. decrease in the percept of spatial acuity. Inhibition due to same-site 200 Hz vibration may play a role in limiting the spatial extent of the cortical activity In a previously published report, Vierck and Jones [2] due to flutter stimulation, creating a sharper and more found that two-point discrimination is improved when finely tuned response, suggesting improved spatial acuity. the stimuli applied to the skin are oscillated versus static (not oscillated). Consequently, they proposed a model of The finding in previous OIS imaging experiments in cats how spatial acuity improved with oscillating versus static that high-frequency skin stimulation is accompanied by a probes. In their report, Vierck and Jones [2] postulated contralateral absorbance increase in area SII and, simulta- that receptive fields in SI were smaller as a result of the neously, by a decline in absorbance in SI in the same hem- oscillating stimulus condition, and that smaller receptive isphere led Tommerdahl et al. [7] to consider the fields were less likely to overlap with one another, and possibility that activity in the corticocortical connections thus, spatial acuity could improve as a result of changing that link SII with SI in the same hemisphere [15,16] leads stimulus conditions. We propose to extend that model by to suppression/inhibition of SI during high-frequency suggesting that the two-point limen is highly correlated skin stimulation. Insofar as the detailed mechanism by with improvements in contrast between peaks of which SII might suppress/inhibit SI, the most straightfor- neuronal activity in SI that are evoked by stimulation of ward possibility (first suggested by Hirsch and Gilbert) two adjacent or near-adjacent points on the skin. Figure 6 [17] is that long-range corticocortical (i.e., SII→SI) summarizes the effect that modification of the stimulus inhibition results from the distinct axonal termination conditions, as reported in this paper, has on our proposed patterns of the local inhibitory neurons in SI. That is, model of SI activity. It should be noted that this concep- because the two major types of local inhibitory cells in the tual model has been influenced by recent findings about upper layers of somatosensory cortex (basket and chande- the SI cortical response to skin stimulation [8,10,12]. lier cells) [18] terminate on cell bodies and initial seg- ments of pyramidal cells, and either do not establish When stimuli consisting of two points are oscillated on synaptic contacts with other inhibitory cells (this is the the skin at low-frequency 25 Hz flutter at distant sites, the case for chandelier cells), or terminate only on the den- peaks of SI response are distinct and non-overlapping drites of inhibitory neurons (characteristic of basket cells), (Figure 6a). Thus, the subject is easily able to discriminate a strong excitatory input from another cortical area (e.g., between the two points. As the points are positioned at the input that SI presumably receives from SII at only a stimulus sites that are closer together, the peaks of brief delay after the onset of high frequency skin stimula- response begin to overlap (Figure 6b), and because the tion) should evoke an inhibitory process in the SI region peaks of activity are no longer easily distinguishable, the that receives the upper layer input, and the inhibition two-point limen is increased (i.e., spatial acuity is worse). should be selectively expressed on pyramidal cells. Adding a same-site high-frequency 200 Hz vibration to the flutter stimuli ("complex" stimuli) has been shown to reduce the spatial extent of the peaks of response in SI Page 8 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 Model of predic Figure 6 ted SI cortical activity in response to specific conditions of tactile stimulation Model of predicted SI cortical activity in response to specific conditions of tactile stimulation. This model is an extension of the Vierck and Jones model (1970) on two-point receptive fields. a. When stimuli consisting of two points are oscillated on the skin at low-frequency 25 Hz flutter at distant sites, the peaks of SI response are distinct and non-overlapping, and therefore the sub- ject is easily able to discriminate between the two points. b. As the points are positioned at stimulus sites that are closer together, the peaks begin to overlap. Because the peaks are no longer easily distinguishable, discriminability is reduced. c. Add- ing a same-site high-frequency 200 Hz vibration to the flutter stimuli ("complex" stimuli) has been shown to reduce the spatial extent of the peaks of response in SI and, as found in the present study, would make it easier to distinguish between two points on the skin. d. Presentation of a stimulus at the same skin site on the unattended hand would reduce the magnitude of SI response by flutter stimulation. This reduction in magnitude of SI response would consequently lead to a reduction in the clar- ity (or contrast) between the activity evoked by the adjacent, or near-adjacent, cortical regions activated by the two stimuli, and as a result, lead to a decrease in spatial acuity. Page 9 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 [6,8] (Figure 6c) and, as found in the present study, would a single 2 mm diameter probe tip and positioned on the make it easier to distinguish between two points on the hand opposite the TPS in a similar fashion. skin. Presentation of a stimulus at the same skin site on the unattended hand would, predictably, reduce the mag- The subject was seated in a chair with arms placed com- nitude of SI response by flutter stimulation [10]. This fortably on a table surface. Both arms were placed on X- reduction in magnitude of cortical response would conse- ray bags filled with glass beads. The investigators molded quently lead to a reduction in the clarity (or contrast) the bags to fit the contours of the subject's arms, and when between the activity evoked by the adjacent, or near-adja- the subject was comfortable and the arms positioned cent, cortical regions activated by the two stimuli (Figure appropriately to allow unimpeded access of the stimula- 6d), and as a result, lead to a decrease in spatial acuity. tor to the center of the dorsal surfaces of each hand, the bags were made rigid by evacuating them of air (achieved by connecting the bag to a vacuum line). In this way the Conclusion In this paper, we propose a model that predicts a correla- arms were maintained in a comfortable but stable posi- tion between SI cortical activity and spatial acuity. Spatial tion for the full duration of the experimental session. The acuity, as measured by the two-point limen, can be mod- subject was unable to see either the experimenter or the ified by changing stimulus conditions that would be pre- stimulator and stimulus-control instrumentation. White dicted to have an impact on the SI cortical response. In noise presented via headphones eliminated potential particular, while vibration has the effect of reducing the auditory cues. A micrometer permitted the stimulator spatial extent of SI cortical response normally evoked by transducers and probe assembly to be lowered towards flutter, such as when a vibrotactile stimulus comprised of the predefined skin sites. The micrometer position at both flutter and vibration is delivered to the skin, it also which the digital display on the stimulator controllers reg- has the effect of improving a subject's ability to discrimi- istered a 0.1–0.2 g change in resistive force was interpreted nate between two points on the skin. Presumably, this as the point at which the stimulator probes made initial occurs as a result of vibration decreasing the spatial extent contact with the skin. of the SI cortical response. Alternatively, stimulus condi- tions that are known to reduce the magnitude of the SI A tracking protocol was used to conduct a two-point cortical response without changing the shape of response, limen test, which determines the "least two-point such as when a second and simultaneous stimulus is separation at which the subject feels (has the subjective delivered to a homotopic skin site on the opposite unat- impression of) two points," [20] at the dorsal surface of tended hand, result in a reduction in spatial discrimina- the right hand. The hand dorsum was chosen because the tion. While SI is regarded as playing a major role in two- innervation density at this site coincided with optimal res- point discrimination, this study provides evidence that olution and separation capabilities of the TPS, and also other cortical areas that are connected to SI (such as SII) because the surface is relatively flat, reducing confounds contribute importantly to SI's ability to differentially of skin curvature present at other potential sites of stimu- respond to closely spaced tactile stimuli. lation. Previous studies indicate that response to tactile acuity tests on the hand dorsum is similar to that on the fingertip, suggesting the dorsum to be a suitable site for Materials & methods Five naïve subjects (21–32 years in age) participated in such tests as well [21]. The subject was instructed to attend this psychophysical study. All procedures were reviewed to the two-point stimulus presented by the TPS on the and approved in advance by an institutional review board. tested hand throughout experimentation. For each run, the two probe tips were initially spaced 30 mm apart. The Sinusoidal vertical skin displacement stimuli were deliv- stimuli were presented to the skin simultaneously for 1 ered using the Cantek Metatron CS-525 vertical displace- sec at an indentation of 500 µm and then completely ment stimulator (Cantek Metatron Corp., Canonsburg, removed from the skin for 1 sec at an offset of -500 µm. PA). The stimulator made contact with the skin via the The subject was given these two seconds to report feeling two tips of the Two-Point Stimulator (TPS) attachment one or two points using a footswitch – no press for one (2.5 cm long, diameter 2 mm) fitted to the terminal end point; a single press for two points. When two points were of the moving shaft of the stimulator transducer. The TPS detected, the two probe tips moved closer together by a is described in detail in a separate report [1]. An adjustable step (1 step = 1 mm); when only one point was detected, mechanical arm with lockable joints mounted to a free- the two points moved farther apart by a step. The probe standing, rigid platform (fabricated locally) enabled con- tips remained off the skin for the tip movement duration venient adjustment and maintenance of stimulus posi- of 1 sec, thus the inter-stimulus interval lasted for a total tion. A second identical Cantek stimulator, implemented of 2 sec. This process was repeated until a threshold could in trials that required bilateral stimulation, was fitted with be determined, usually around 30 trials, hence a single run took approximately 90 sec. The inter-run interval was Page 10 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 14. Sherrick CE, Cholewiak RW, Collins AA: The localization of low- 60 sec in duration. The two-point limen was measured and high frequency vibrotactile stimuli. J Acoust Soc Am 1990, under four conditions of frequency and amplitude: unilat- 88(1):169-179. eral 25 Hz-100 µm, unilateral 25 Hz-100 µm + 200 Hz-20 15. Burton H, Fabri M: Ipsilateral intracortical connections of phys- iologically defined cutaneous representations in areas 3b and µm ("complex"), bilateral stimulation of 25 Hz-100 µm 1 of macaque monkeys: projections in the vicinity of the cen- on both hands, and bilateral stimulation of 25 Hz-100 tral sulcus. J Comp Neurol 1995, 355:508-538. 16. Alloway KD, Burton H: Homotypical ipsilateral cortical projec- µm on the attended hand and 200 Hz-20 µm on the tions between somatosensory areas I and II in the cat. Neu- opposite unattended hand. In a session, four runs were roscience 1985, 14(1):15-35. conducted, each with one of the aforementioned stimulus 17. Hirsch JA, Gilbert CD: Synaptic physiology of horizontal con- nections in the cat's visual cortex. J Neurosci 1991, conditions. In the bilateral conditions, stimuli were 11:1800-1809. applied by a single timing mechanism and thus were pre- 18. Jones EG: Varieties and distribution of non-pyramidal cells in sented to the skin in phase and synchrony. Order of stim- the somatic sensory cortex of the squirrel monkey. J Comp Neurol 1975, 160:205-267. ulus conditions within a session was randomized and 19. Braun C, Hess H, Burkhardt M, Wuhle A, Preissl H: The right hand varied for each subject. knows what the left hand is feeling. Exp Brain Res 2005, 162(3):366-373. 20. Johnson KO, Phillips JR: Tactile spatial resolution. I. Two-point Authors' contributions discrimination, gap detection, grating resolution, and letter VT conducted the experiments, analyzed the data and recognition. J Neurophysiol 1981, 46(6):1177-1192. 21. Schlereth T, Magerl W, Treede R: Spatial discrimination thresh- drafted the manuscript. RD had a role in the conduct and olds for pain and touch in human hairy skin. Pain 2001, 92(1– design of the experiments. MT was involved with the 2):187-194. design of the experiments and the preparation of the manuscript. Acknowledgements Supported, in part, by NIH R01 grant NS043375 (M. Tommerdahl, P.I.). References 1. Tannan V, Dennis RG, Tommerdahl M: A novel device for deliver- ing two-site vibrotactile stimuli to the skin. J Neurosci Methods 2005, 147:75-81. 2. Vierck CJ, Jones MB: Influences of low and high frequency oscil- lation upon spatio-tactile resolution. Physiol Behav 1970, 5(12):1431-1435. 3. Mountcastle VB, Darian-Smith I: Neural mechanisms in som- esthesia. In Medical Physiology Volume 2. 12th edition. Edited by: Mountcastle VB. St. Louis: Mosby; 1968:1372-1423. 4. LaMotte RH, Mountcastle VB: Capacities of humans and mon- keys to discriminate between vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychophysical measurements. J Neurophysiol 1975, 38:539-559. 5. LaMotte RH, Mountcastle VB: Disorders in somesthesis follow- ing lesions of parietal lobe. J Neurophysiol 1979, 42:400-419. 6. Tommerdahl M, Delemos KA, Whitsel BL, Favorov OV, Metz CB: Response of anterior parietal cortex to cutaneous flutter and vibration. J Neurophysiol 1999, 82(1):16-33. 7. Tommerdahl M, Whitsel BL, Favorov OV, Metz CB, O'Quinn BL: Responses of contralateral SI and SII in cat to same site cuta- neous flutter versus vibration. J Neurophysiol 1999, 82:1982-1992. 8. Tommerdahl M, Favorov OV, Whitsel BL: Effects of high-fre- quency skin stimulation on SI cortex: mechanisms and func- tional implications. Somatosens Mot Res in press. 9. Whitsel BL, Kelly EF, Xu M, Tommerdahl M, Quibrera M: Fre- Publish with Bio Med Central and every quency-dependent response of SI RA-class neurons to vibro- scientist can read your work free of charge tactile stimulation of the receptive field. Somatosens Mot Res 2001, 18:263-285. "BioMed Central will be the most significant development for 10. Tommerdahl M, Simons SB, Chiu JS, Favorov OV, Whitsel BL: disseminating the results of biomedical researc h in our lifetime." Response of SI cortex to ipsilateral, contralateral and bilat- Sir Paul Nurse, Cancer Research UK eral flutter stimulation in the cat. BMC Neurosci 2005, 6(1):29. 11. Vega-Bermudez F, Johnson KO: Fingertip skin conformance Your research papers will be: accounts, in part, for differences in tactile spatial acuity in available free of charge to the entire biomedical community young subjects, but not for the decline in spatial acuity with aging. Percept Psychophys 2004, 66(1):60-67. peer reviewed and published immediately upon acceptance 12. Simons SB, Tannan V, Chiu J, Favorov OV, Whitsel BL, Tommerdahl cited in PubMed and archived on PubMed Central M: Amplitude-dependency of response of SI cortex to vibro- tactile stimulation. BMC Neurosci 2005, 6(1):43. yours — you keep the copyright 13. Summers IR, Chanter CM: A broadband tactile array on the BioMedcentral Submit your manuscript here: fingertip. J Acoust Soc Am 2002, 112(5):2118-2126. http://www.biomedcentral.com/info/publishing_adv.asp Page 11 of 11 (page number not for citation purposes) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral and Brain Functions Springer Journals

Stimulus-dependent effects on tactile spatial acuity

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Springer Journals
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Copyright © 2005 by Tannan et al; licensee BioMed Central Ltd.
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Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
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Abstract

Background: Previous studies have shown that spatio-tactile acuity is influenced by the clarity of the cortical response in primary somatosensory cortex (SI). Stimulus characteristics such as frequency, amplitude, and location of tactile stimuli presented to the skin have been shown to have a significant effect on the response in SI. The present study observes the effect of changing stimulus parameters of 25 Hz sinusoidal vertical skin displacement stimulation ("flutter") on a human subject's ability to discriminate between two adjacent or near-adjacent skin sites. Based on results obtained from recent neurophysiological studies of the SI response to different conditions of vibrotactile stimulation, we predicted that the addition of 200 Hz vibration to the same site that a two-point flutter stimulus was delivered on the skin would improve a subject's spatio-tactile acuity over that measured with flutter alone. Additionally, similar neurophysiological studies predict that the presence of either a 25 Hz flutter or 200 Hz vibration stimulus on the unattended hand (on the opposite side of the body from the site of two-point limen testing – the condition of bilateral stimulation – which has been shown to evoke less SI cortical activity than the contralateral-only stimulus condition) would decrease a subject's ability to discriminate between two points on the skin. Results: A Bekesy tracking method was employed to track a subject's ability to discriminate between two-point stimuli delivered to the skin. The distance between the two points of stimulation was varied on a trial-by-trial basis, and several different stimulus conditions were examined: (1) The "control" condition, in which 25 Hz flutter stimuli were delivered simultaneously to the two points on the skin of the attended hand, (2) the "complex" condition, in which a combination of 25 Hz flutter and 200 Hz vibration stimuli were delivered to the two points on the attended hand, and (3) a "bilateral" condition, in which 25 Hz flutter was delivered to the two points on the attended hand and a second stimulus (either flutter or vibration) was delivered to the unattended hand. The two-point limen was reduced (i.e., spatial acuity was improved) under the complex stimulus condition when compared to the control stimulus condition. Specifically, whereas adding vibration to the unilateral two-point flutter stimulus improved spatial acuity by 20 to 25%, the two-point limen was not significantly affected by substantial changes in stimulus amplitude (between 100 – 200 µm). In contrast, simultaneous stimulation of the unattended hand (contralateral to the attended site), impaired spatial acuity by 20% with flutter stimulation and by 30% with vibration stimulation. Conclusion: It was found that the addition of 200 Hz vibration to a two-point 25 Hz flutter stimulus significantly improved a subject's ability to discriminate between two points on the skin. Since previous studies showed that 200 Hz vibration preferentially evokes activity in cortical area SII and reduces or inhibits the spatial extent of activity in SI in the same hemisphere, the findings in this paper raise the possibility that although SI activity plays a major role in two-point discrimination on the skin, influences relayed to SI from SII in the same hemisphere may contribute importantly to SI's ability to differentially respond to stimuli applied to closely spaced skin points on the same side of the body midline. Page 1 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 have been found in the non-human primate (unpub- Introduction Recently, we reported the development of a semi-auto- lished observations). This led us to the prediction that, mated method for measuring a human subject's ability to because of the decrease in prominence of the two peaks of discriminate between two points on the skin [1]. In that neuronal activity in SI evoked and consequently, the study, a Two-Point Stimulator (TPS) was employed to reduction in the spatial clarity between those peaks of cor- deliver tactile stimuli simultaneously to two separate skin tical activity, a subject's two-point limen would increase sites. Since distance between the two points of the TPS can (indicating reduced spatial acuity) with the addition of a be adjusted on a trial-by-trial basis, it was possible to stimulus to the unattended hand. employ a Bekesy tracking method to determine a subject's two-point limen under several different conditions of Results two-point stimulation. Two-point stimuli were presented Bekesy tracking algorithms were used to find a subject's to the skin under static conditions (two probes simply two-point limen at the dorsal surface of the right hand pressed into the skin), in the presence of flutter stimula- under four different stimulus conditions. Exemplary tion (probes oscillated at 25 Hz as they were pressed into results for a single session (four runs) of a subject are the skin), or in the presence of vibration (probes oscil- shown in Figure 1. The two-point limen of the subject was lated at 200 Hz). The results duplicated the finding of tracked for two points delivered simultaneously and oscil- Vierck and Jones [2] that demonstrated that oscillating the lated at 25 Hz on the attended hand (AH). The data pre- two probes improved a subject's spatial acuity (as meas- sented indicate that under this condition the subject was ured by the two-point limen). Furthermore, both our able to detect the presence of two points at a separation of study and the Vierck and Jones report showed that spatial approximately 19 mm (average response for the last five acuity is better in the 25 Hz stimulus condition than in the trials). In a second run (the "complex" stimulus condi- 200 Hz stimulus condition. tion), the two-point limen was tracked under identical conditions as the first run, with the exception that the 25 Mountcastle and Darian-Smith [3] proposed that a sub- Hz stimulus waveform was delivered with an additional ject's ability to spatially discriminate between two points 200 Hz vibration on the attended hand (see Methods). on the skin would be dependent on the lateral inhibition The addition of the 200 Hz vibration to the 25 Hz flutter that enables the formation of the peaks of neuronal activ- resulted in a decrease in the two-point limen to approxi- ity in SI cortex. Additionally, LaMotte and Mountcastle mately 16.4 mm. In the two other conditions, the two- [4,5] asserted that the capacity of a subject to accurately point limen was tracked to a two-point 25 Hz flutter stim- localize a flutter stimulus on the skin is determined by the ulus on the attended hand, under identical conditions as locus and clarity of the flutter-evoked neuron population the first run, but with the addition of a simultaneous 25 response within the topographically organized SI net- Hz flutter or 200 Hz vibration stimulus to the opposite, work. If this is the case, then the ability of a subject to dis- unattended hand (UH). Interestingly, in both cases, stim- criminate between two points would improve if the locus ulation of the unattended hand impaired the subjects' of the responses in SI to the stimuli at the two correspond- ability to discriminate between two points on the ing skin sites were more clearly defined – i.e., if the spatial attended hand, and thus, the two-point limen actually extent of the response in SI to a point stimulus waslimited increased to values of approximately 22 mm and 24 mm or reduced. Observations by Tommerdahl and colleagues for 25 Hz and 200 Hz unattended conditions, respec- demonstrated that the SI response to a complex stimulus tively. To summarize, the detection of two points pre- (one comprised of both flutter and vibration) is spatially sented simultaneously with flutter was improved with constrained when compared to the response to flutter same-site vibration and degraded with the addition of alone [6-9]. In other words, the SI response evoked by a either a flutter or vibration stimulus on the opposite, complex stimulus is smaller in spatial extent than that unattended hand. evoked by 25 Hz flutter alone. Thus, based on the effect that same-site vibration has on the SI response to flutter, To determine subject consistency of the above findings, we were led to the prediction that vibration, if presented the tracking data collected under each condition for an simultaneously at the same sites as two-point flutter stim- individual subject were averaged. The data were normal- uli (i.e., as a complex stimulus comprised of 25 Hz and ized to the flutter condition since the primary objective of 200 Hz components), would improve a subject's ability to this study was to determine the effect of vibration on the discriminate between two points. Alternatively, recent response normally evoked by two-point flutter stimula- findings comparing the SI activity evoked by different tion. Thus, the two-point limen for the flutter condition conditions of contralateral, ipsilateral and bilateral stimu- was defined as the value "1" and all other distances are lation in the cat show that the magnitude of response in plotted as a proportion of the values obtained under the SI evoked by contralateral stimulation is reduced in the flutter condition [1]. The normalized average two-point presence of an ipsilateral stimulus [10]. Similar results limen plot for one subject is displayed in Figure 2. Note Page 2 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 A Figure 1 tracking protocol was used to conduct a two-point limen threshold test A tracking protocol was used to conduct a two-point limen threshold test. Separation between the two probe tips on the attended hand (AH) versus time was observed under four conditions of stimulation. One condition consisted of 25 Hz flutter applied by the TPS on the AH. In a second condition, the two tips were applied to the AH by a complex stimulus (25 Hz+200 Hz). For the other two conditions, 25 Hz flutter was applied to the AH with either a 25 Hz flutter or 200 Hz vibration stimulus applied simultaneously to the unattended hand (UH). A single trial consisted of stimuli presented to the skin for 1 sec, and then completely removed from the skin for an inter-stimulus interval of 2 sec. Each run consisted of 30 trials, or a duration of 90 sec total. that the two-point limen was reduced (i.e., spatial acuity two-point limen values that were approximately 30% was improved) for the complex condition – the two-point higher than the control condition. limen tracks at approximately 80% of the values measured under the flutter condition. In contrast, the two-point To determine the across-subject consistency of the above limen was larger (i.e., spatial acuity is worse) for both findings, the data normalization process applied to the bilateral conditions. In the case in which the opposite or single subject case, as shown in Figure 2 and described unattended hand was presented with a simultaneous 25 above, was repeated for data collected under each condi- Hz flutter stimulus, the two-point limen tracks approxi- tion across all subjects. Normalized and averaged data are mately 20% higher than the control (attended hand only) shown in Figure 3. Similar to the data presented in Figure condition. Similarly, applying a 200 Hz vibration stimu- 2, the two-point limen for the complex condition tracked lus simultaneously to the unattended hand resulted in between 75 and 80% of that measured under the flutter Page 3 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 Figure 2 Average of two-point limen tracking, under all conditions, for one exemplary subject Average of two-point limen tracking, under all conditions, for one exemplary subject. All distances are normalized to the two- point distance recorded under the attended hand (AH) 25 Hz flutter condition. Standard error bars demonstrate that across- session variability for the two-point limen tracking method is fairly consistent. condition, indicating a 20–25% improvement in spatial dition, or when vibration was presented with flutter, by acuity resulting from the presence of vibration during the dual-site stimuli on the attended hand. Alternatively, the flutter stimulus driving the TPS on the attended hand. two-point limen increased when a second, simultaneous Alternatively, tracking of the two-point limen showed an stimulus was added to the unattended hand – approxi- increase of approximately 20% and 30% for the condi- mately 20% for the 25 Hz flutter condition and 30% for tions in which the unattended hand was stimulated with 200 Hz vibration condition. Standard error bars demon- flutter and vibration, respectively. strate that across-subject variability for the two-point limen tracking method is fairly consistent. ANOVA testing In order to more directly compare the responses measured was conducted on this data with the null hypothesis that under each of the stimulus conditions, the tracking values the mean under the control flutter condition is signifi- obtained from the last five trials across all subjects was cantly different than the means obtained under the three averaged and normalized to the flutter condition (Figure test conditions. The means for the bilateral conditions of 4). Again, it is apparent that the two-point limen values unattended hand 25 Hz (F = 47.7; p < 0.00000001) and decreased by approximately 20% under the complex con- unattended hand 200 Hz (F = 76.3; p < 0.00000001), as Page 4 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 A Figure 3 verage of two-point limen tracking across all subjects Average of two-point limen tracking across all subjects. All distances are normalized to the two-point distance recorded under the attended hand (AH) 25 Hz flutter condition. Standard error bars demonstrate that across-subject variability for the two- point limen tracking method is fairly consistent. well as the complex condition (F = 27.6; p < 0.00001) are ner as the previous results (see Figure 5). In both the 150 significantly different from the mean under the flutter and 200 µm conditions, the two-point limen oscillated condition. approximately within 10% of that observed at the 100 µm condition, suggesting that there was no consistent effect To ensure that the enhanced acuity of a subject under the on the two-point limen due to the increased amplitude of complex stimulus condition was not due simply to the the complex stimulus and that the effect seen under the increased amplitude that resulted from adding vibration complex condition was most likely attributable to the to a flutter stimulus (which resulted in a stimulus ampli- additional high-frequency component. tude of 120 µm), the two-point limen was tracked on the attended hand at 25 Hz flutter of varying amplitudes. Spe- Discussion cifically, a separate series of sessions were conducted to In the present study, we observed stimulus-dependent track and compare the two-point limen for the amplitudes effects on two-point tracking of a flutter stimulus at the of 100, 150, and 200 µm in the flutter-only condition. The dorsal surface of the attended hand. The two-point limen results were normalized to the distances observed under was reduced (spatial acuity was improved) with a complex the 100 µm condition and were plotted in the same man- stimulus that consisted of 25 Hz flutter and 200 Hz Page 5 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 A Figure 4 verage of last five trials of two-point limen tracking across all subjects, with standard error bars Average of last five trials of two-point limen tracking across all subjects, with standard error bars. All distances are normalized to the two-point distance recorded under the attended hand (AH) flutter condition. vibration components. Specifically, it was found that add- within the amplitude range used, there were no significant ing vibration to the unilateral two-point flutter stimulus differences in the two-point limen. This is also consistent improved spatial acuity by 20 to 25%. When the amplitude with the idea that increasing amplitude of a stimulus does of the unilateral two-point flutter stimulus was signifi- not increase the spatial extent of its cortical response – a cantly varied (between 100 – 200 µm), the two-point finding recently reported [12]. In that report, observations limen was not affected. Simultaneous stimulation of the obtained from imaging the optical intrinsic signal in non- hand contralateral to the attended site, however, impaired human primates showed that higher amplitudes of stimu- or reduced spatial acuity by 20% with a flutter stimulus and lation with a 25 Hz flutter stimulus in the amplitude range 30% with a vibratory stimulus. studied (50–400 µm at a frequency of 25 Hz) did not pro- duce larger areas of cortical activation in primary somato- Vega-Bermudez and Johnson [11], using grating orienta- sensory cortex (SI). Rather, the spatial extent of the tion studies, cited the importance of skin deformation as cortical patterns of activation evoked by the flutter stimu- a factor affecting spatial acuity. For this reason, we consid- lus was limited. Simons et al. postulated that the cortical ered the possibility that enhanced spatial acuity with a response is sculpted or refined by lateral inhibition, complex stimulus may be due to the fact that adding thereby limiting changes in spatial extent [12]. These find- vibration to the flutter stimulus introduces another ampli- ings are consistent with the idea that the spatial extent of tude component, thereby increasing the overall magni- the SI response evoked by each of the point stimuli plays tude of the stimulus. Results from our study showed that, a role in a subject's ability to discriminate between two Page 6 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 A a Figure 5 tten verage of two- ded hand atpoint limen tracking acr amplitudes of 100 µm, 150 oss all subjects for cont µm, or 200 µm rol conditions: 25 Hz flutter stimulus applied by the TPS to the Average of two-point limen tracking across all subjects for control conditions: 25 Hz flutter stimulus applied by the TPS to the attended hand at amplitudes of 100 µm, 150 µm, or 200 µm. All distances are normalized to the two-point distance recorded under the 25 Hz-100 µm condition. stimulus sites on the skin, since changing the amplitude of However, Summers and Chanter also stated that this type a flutter stimulus has little effect on either the spatial of interpretation (that the addition of high-frequency extent of the SI response in primates or on the two-point vibration to a lower-frequency stimulus results in limen observations made in this report. improvement in perception of that stimulus) was prob- lematic because of the known differences between mech- Summers and Chanter [13] reported results on tactile acu- anoreceptors [13]. Previous studies had established the ity in the fingertip in response to stimuli presented by a fact that spatial acuity was worse at high frequencies (in broadband tactile array. They found that localization of a the Pacinian range) than at low frequencies (RA/SA range) 40 Hz target stimulus was improved with the addition of [1,2,14]. However, if spatial acuity can be attributed to the a 320 Hz background stimulus (which surrounded the tar- spatial clarity between regions of cortical activity as get) compared to that with a 40 Hz background stimulus. LaMotte and Mountcastle [4] proposed, then the cortico- Page 7 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 cortical interactions that result from the condition of A recent report described that the ability to localize a stim- simultaneous flutter and vibration [8] would ulus on the fingertips of one hand may be impaired with undoubtedly have an effect on measures of spatial acuity. the interference of a similar stimulus on a fingertip of the Flutter stimuli, such as the ones presented in this study, opposite hand [19], suggesting that spatial acuity may be are known to evoke significant and sustained activity in SI worse with bilateral stimulation than with unilateral stim- cortex. Skin stimulation at 200 Hz, on the other hand, has ulation under certain conditions. In a separate study, we been shown to reduce the spatial extent of SI response reported that the SI cortical response to contralateral skin normally evoked by a 25 Hz flutter stimulus [6-9]. stimulation was reduced when an identical stimulus was presented simultaneously to the ipsilateral (mirror image) Tommerdahl et al. [6] compared the intrinsic signal skin site [10]. Specifically, Tommerdahl and colleagues evoked in areas 3b/1 by 25 Hz skin stimulation to the found that the magnitude of response in SI to bilateral intrinsic signal evoked by a same-site skin stimulus stimulation was 30–35% smaller than the response containing both 25 and 200 Hz sinusoidal components (a evoked by a contralateral flutter stimulus. This finding led "complex waveform stimulus"). Such experiments us to postulate that, since contralateral SI is recognized as revealed that the increase in absorbance evoked in areas the cortical region most responsible for spatial localiza- 3b/1 by a stimulus having both 25 and 200 Hz compo- tion [4,5], a reduction in the magnitude of the contralat- nents was substantially smaller than the increase in eral SI response – via ipsilateral stimulation – could cause absorbance evoked by "pure" 25 Hz stimulation of the a reduction in spatial acuity. Results from the present same skin site. It was concluded that within a brief time study support this hypothesis, suggesting that bilateral after stimulus onset, 200 Hz skin stimulation evokes a stimulation of two homologous body parts leads to a powerful inhibitory action on area 3b/1 QA neurons. decrease in the percept of spatial acuity. Inhibition due to same-site 200 Hz vibration may play a role in limiting the spatial extent of the cortical activity In a previously published report, Vierck and Jones [2] due to flutter stimulation, creating a sharper and more found that two-point discrimination is improved when finely tuned response, suggesting improved spatial acuity. the stimuli applied to the skin are oscillated versus static (not oscillated). Consequently, they proposed a model of The finding in previous OIS imaging experiments in cats how spatial acuity improved with oscillating versus static that high-frequency skin stimulation is accompanied by a probes. In their report, Vierck and Jones [2] postulated contralateral absorbance increase in area SII and, simulta- that receptive fields in SI were smaller as a result of the neously, by a decline in absorbance in SI in the same hem- oscillating stimulus condition, and that smaller receptive isphere led Tommerdahl et al. [7] to consider the fields were less likely to overlap with one another, and possibility that activity in the corticocortical connections thus, spatial acuity could improve as a result of changing that link SII with SI in the same hemisphere [15,16] leads stimulus conditions. We propose to extend that model by to suppression/inhibition of SI during high-frequency suggesting that the two-point limen is highly correlated skin stimulation. Insofar as the detailed mechanism by with improvements in contrast between peaks of which SII might suppress/inhibit SI, the most straightfor- neuronal activity in SI that are evoked by stimulation of ward possibility (first suggested by Hirsch and Gilbert) two adjacent or near-adjacent points on the skin. Figure 6 [17] is that long-range corticocortical (i.e., SII→SI) summarizes the effect that modification of the stimulus inhibition results from the distinct axonal termination conditions, as reported in this paper, has on our proposed patterns of the local inhibitory neurons in SI. That is, model of SI activity. It should be noted that this concep- because the two major types of local inhibitory cells in the tual model has been influenced by recent findings about upper layers of somatosensory cortex (basket and chande- the SI cortical response to skin stimulation [8,10,12]. lier cells) [18] terminate on cell bodies and initial seg- ments of pyramidal cells, and either do not establish When stimuli consisting of two points are oscillated on synaptic contacts with other inhibitory cells (this is the the skin at low-frequency 25 Hz flutter at distant sites, the case for chandelier cells), or terminate only on the den- peaks of SI response are distinct and non-overlapping drites of inhibitory neurons (characteristic of basket cells), (Figure 6a). Thus, the subject is easily able to discriminate a strong excitatory input from another cortical area (e.g., between the two points. As the points are positioned at the input that SI presumably receives from SII at only a stimulus sites that are closer together, the peaks of brief delay after the onset of high frequency skin stimula- response begin to overlap (Figure 6b), and because the tion) should evoke an inhibitory process in the SI region peaks of activity are no longer easily distinguishable, the that receives the upper layer input, and the inhibition two-point limen is increased (i.e., spatial acuity is worse). should be selectively expressed on pyramidal cells. Adding a same-site high-frequency 200 Hz vibration to the flutter stimuli ("complex" stimuli) has been shown to reduce the spatial extent of the peaks of response in SI Page 8 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 Model of predic Figure 6 ted SI cortical activity in response to specific conditions of tactile stimulation Model of predicted SI cortical activity in response to specific conditions of tactile stimulation. This model is an extension of the Vierck and Jones model (1970) on two-point receptive fields. a. When stimuli consisting of two points are oscillated on the skin at low-frequency 25 Hz flutter at distant sites, the peaks of SI response are distinct and non-overlapping, and therefore the sub- ject is easily able to discriminate between the two points. b. As the points are positioned at stimulus sites that are closer together, the peaks begin to overlap. Because the peaks are no longer easily distinguishable, discriminability is reduced. c. Add- ing a same-site high-frequency 200 Hz vibration to the flutter stimuli ("complex" stimuli) has been shown to reduce the spatial extent of the peaks of response in SI and, as found in the present study, would make it easier to distinguish between two points on the skin. d. Presentation of a stimulus at the same skin site on the unattended hand would reduce the magnitude of SI response by flutter stimulation. This reduction in magnitude of SI response would consequently lead to a reduction in the clar- ity (or contrast) between the activity evoked by the adjacent, or near-adjacent, cortical regions activated by the two stimuli, and as a result, lead to a decrease in spatial acuity. Page 9 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 [6,8] (Figure 6c) and, as found in the present study, would a single 2 mm diameter probe tip and positioned on the make it easier to distinguish between two points on the hand opposite the TPS in a similar fashion. skin. Presentation of a stimulus at the same skin site on the unattended hand would, predictably, reduce the mag- The subject was seated in a chair with arms placed com- nitude of SI response by flutter stimulation [10]. This fortably on a table surface. Both arms were placed on X- reduction in magnitude of cortical response would conse- ray bags filled with glass beads. The investigators molded quently lead to a reduction in the clarity (or contrast) the bags to fit the contours of the subject's arms, and when between the activity evoked by the adjacent, or near-adja- the subject was comfortable and the arms positioned cent, cortical regions activated by the two stimuli (Figure appropriately to allow unimpeded access of the stimula- 6d), and as a result, lead to a decrease in spatial acuity. tor to the center of the dorsal surfaces of each hand, the bags were made rigid by evacuating them of air (achieved by connecting the bag to a vacuum line). In this way the Conclusion In this paper, we propose a model that predicts a correla- arms were maintained in a comfortable but stable posi- tion between SI cortical activity and spatial acuity. Spatial tion for the full duration of the experimental session. The acuity, as measured by the two-point limen, can be mod- subject was unable to see either the experimenter or the ified by changing stimulus conditions that would be pre- stimulator and stimulus-control instrumentation. White dicted to have an impact on the SI cortical response. In noise presented via headphones eliminated potential particular, while vibration has the effect of reducing the auditory cues. A micrometer permitted the stimulator spatial extent of SI cortical response normally evoked by transducers and probe assembly to be lowered towards flutter, such as when a vibrotactile stimulus comprised of the predefined skin sites. The micrometer position at both flutter and vibration is delivered to the skin, it also which the digital display on the stimulator controllers reg- has the effect of improving a subject's ability to discrimi- istered a 0.1–0.2 g change in resistive force was interpreted nate between two points on the skin. Presumably, this as the point at which the stimulator probes made initial occurs as a result of vibration decreasing the spatial extent contact with the skin. of the SI cortical response. Alternatively, stimulus condi- tions that are known to reduce the magnitude of the SI A tracking protocol was used to conduct a two-point cortical response without changing the shape of response, limen test, which determines the "least two-point such as when a second and simultaneous stimulus is separation at which the subject feels (has the subjective delivered to a homotopic skin site on the opposite unat- impression of) two points," [20] at the dorsal surface of tended hand, result in a reduction in spatial discrimina- the right hand. The hand dorsum was chosen because the tion. While SI is regarded as playing a major role in two- innervation density at this site coincided with optimal res- point discrimination, this study provides evidence that olution and separation capabilities of the TPS, and also other cortical areas that are connected to SI (such as SII) because the surface is relatively flat, reducing confounds contribute importantly to SI's ability to differentially of skin curvature present at other potential sites of stimu- respond to closely spaced tactile stimuli. lation. Previous studies indicate that response to tactile acuity tests on the hand dorsum is similar to that on the fingertip, suggesting the dorsum to be a suitable site for Materials & methods Five naïve subjects (21–32 years in age) participated in such tests as well [21]. The subject was instructed to attend this psychophysical study. All procedures were reviewed to the two-point stimulus presented by the TPS on the and approved in advance by an institutional review board. tested hand throughout experimentation. For each run, the two probe tips were initially spaced 30 mm apart. The Sinusoidal vertical skin displacement stimuli were deliv- stimuli were presented to the skin simultaneously for 1 ered using the Cantek Metatron CS-525 vertical displace- sec at an indentation of 500 µm and then completely ment stimulator (Cantek Metatron Corp., Canonsburg, removed from the skin for 1 sec at an offset of -500 µm. PA). The stimulator made contact with the skin via the The subject was given these two seconds to report feeling two tips of the Two-Point Stimulator (TPS) attachment one or two points using a footswitch – no press for one (2.5 cm long, diameter 2 mm) fitted to the terminal end point; a single press for two points. When two points were of the moving shaft of the stimulator transducer. The TPS detected, the two probe tips moved closer together by a is described in detail in a separate report [1]. An adjustable step (1 step = 1 mm); when only one point was detected, mechanical arm with lockable joints mounted to a free- the two points moved farther apart by a step. The probe standing, rigid platform (fabricated locally) enabled con- tips remained off the skin for the tip movement duration venient adjustment and maintenance of stimulus posi- of 1 sec, thus the inter-stimulus interval lasted for a total tion. A second identical Cantek stimulator, implemented of 2 sec. This process was repeated until a threshold could in trials that required bilateral stimulation, was fitted with be determined, usually around 30 trials, hence a single run took approximately 90 sec. The inter-run interval was Page 10 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2005, 1:18 http://www.behavioralandbrainfunctions.com/content/1/1/18 14. Sherrick CE, Cholewiak RW, Collins AA: The localization of low- 60 sec in duration. The two-point limen was measured and high frequency vibrotactile stimuli. J Acoust Soc Am 1990, under four conditions of frequency and amplitude: unilat- 88(1):169-179. eral 25 Hz-100 µm, unilateral 25 Hz-100 µm + 200 Hz-20 15. Burton H, Fabri M: Ipsilateral intracortical connections of phys- iologically defined cutaneous representations in areas 3b and µm ("complex"), bilateral stimulation of 25 Hz-100 µm 1 of macaque monkeys: projections in the vicinity of the cen- on both hands, and bilateral stimulation of 25 Hz-100 tral sulcus. J Comp Neurol 1995, 355:508-538. 16. Alloway KD, Burton H: Homotypical ipsilateral cortical projec- µm on the attended hand and 200 Hz-20 µm on the tions between somatosensory areas I and II in the cat. Neu- opposite unattended hand. In a session, four runs were roscience 1985, 14(1):15-35. conducted, each with one of the aforementioned stimulus 17. Hirsch JA, Gilbert CD: Synaptic physiology of horizontal con- nections in the cat's visual cortex. J Neurosci 1991, conditions. In the bilateral conditions, stimuli were 11:1800-1809. applied by a single timing mechanism and thus were pre- 18. Jones EG: Varieties and distribution of non-pyramidal cells in sented to the skin in phase and synchrony. Order of stim- the somatic sensory cortex of the squirrel monkey. J Comp Neurol 1975, 160:205-267. ulus conditions within a session was randomized and 19. Braun C, Hess H, Burkhardt M, Wuhle A, Preissl H: The right hand varied for each subject. knows what the left hand is feeling. Exp Brain Res 2005, 162(3):366-373. 20. Johnson KO, Phillips JR: Tactile spatial resolution. I. Two-point Authors' contributions discrimination, gap detection, grating resolution, and letter VT conducted the experiments, analyzed the data and recognition. J Neurophysiol 1981, 46(6):1177-1192. 21. Schlereth T, Magerl W, Treede R: Spatial discrimination thresh- drafted the manuscript. RD had a role in the conduct and olds for pain and touch in human hairy skin. Pain 2001, 92(1– design of the experiments. MT was involved with the 2):187-194. design of the experiments and the preparation of the manuscript. Acknowledgements Supported, in part, by NIH R01 grant NS043375 (M. Tommerdahl, P.I.). References 1. Tannan V, Dennis RG, Tommerdahl M: A novel device for deliver- ing two-site vibrotactile stimuli to the skin. J Neurosci Methods 2005, 147:75-81. 2. Vierck CJ, Jones MB: Influences of low and high frequency oscil- lation upon spatio-tactile resolution. Physiol Behav 1970, 5(12):1431-1435. 3. Mountcastle VB, Darian-Smith I: Neural mechanisms in som- esthesia. In Medical Physiology Volume 2. 12th edition. Edited by: Mountcastle VB. St. Louis: Mosby; 1968:1372-1423. 4. LaMotte RH, Mountcastle VB: Capacities of humans and mon- keys to discriminate between vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychophysical measurements. J Neurophysiol 1975, 38:539-559. 5. LaMotte RH, Mountcastle VB: Disorders in somesthesis follow- ing lesions of parietal lobe. J Neurophysiol 1979, 42:400-419. 6. Tommerdahl M, Delemos KA, Whitsel BL, Favorov OV, Metz CB: Response of anterior parietal cortex to cutaneous flutter and vibration. J Neurophysiol 1999, 82(1):16-33. 7. Tommerdahl M, Whitsel BL, Favorov OV, Metz CB, O'Quinn BL: Responses of contralateral SI and SII in cat to same site cuta- neous flutter versus vibration. J Neurophysiol 1999, 82:1982-1992. 8. Tommerdahl M, Favorov OV, Whitsel BL: Effects of high-fre- quency skin stimulation on SI cortex: mechanisms and func- tional implications. Somatosens Mot Res in press. 9. Whitsel BL, Kelly EF, Xu M, Tommerdahl M, Quibrera M: Fre- Publish with Bio Med Central and every quency-dependent response of SI RA-class neurons to vibro- scientist can read your work free of charge tactile stimulation of the receptive field. Somatosens Mot Res 2001, 18:263-285. "BioMed Central will be the most significant development for 10. Tommerdahl M, Simons SB, Chiu JS, Favorov OV, Whitsel BL: disseminating the results of biomedical researc h in our lifetime." Response of SI cortex to ipsilateral, contralateral and bilat- Sir Paul Nurse, Cancer Research UK eral flutter stimulation in the cat. BMC Neurosci 2005, 6(1):29. 11. Vega-Bermudez F, Johnson KO: Fingertip skin conformance Your research papers will be: accounts, in part, for differences in tactile spatial acuity in available free of charge to the entire biomedical community young subjects, but not for the decline in spatial acuity with aging. Percept Psychophys 2004, 66(1):60-67. peer reviewed and published immediately upon acceptance 12. Simons SB, Tannan V, Chiu J, Favorov OV, Whitsel BL, Tommerdahl cited in PubMed and archived on PubMed Central M: Amplitude-dependency of response of SI cortex to vibro- tactile stimulation. BMC Neurosci 2005, 6(1):43. yours — you keep the copyright 13. Summers IR, Chanter CM: A broadband tactile array on the BioMedcentral Submit your manuscript here: fingertip. J Acoust Soc Am 2002, 112(5):2118-2126. http://www.biomedcentral.com/info/publishing_adv.asp Page 11 of 11 (page number not for citation purposes)

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