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Background: Many human neuroimaging investigations on recognition memory employ verbal instructions to direct subject's attention to a stimulus attribute. But do the same or a similar neurophysiological process occur during nonverbal experiences, such as those involving contingency-shaped responses? Establishing the spatially distributed neural network underlying recognition memory for instructed stimuli and operant, contingency-shaped (i.e., discriminative) stimuli would extend the generality of contemporary domain-general views of recognition memory and clarify the involvement of declarative memory processes in human operant behavior. Methods: Fifteen healthy adults received equivalent amounts of exposure to three different stimulus sets prior to neuroimaging. Encoding of one stimulus set was prompted using instructions that emphasized memorizing stimuli (Instructed). In contrast, encoding of two additional stimulus sets was prompted using a GO/NO-GO operant task, in which contingencies shaped appropriate GO and NO-GO responding. During BOLD functional MRI, subjects completed two recognition tasks. One required passive viewing of stimuli. The second task required recognizing whether a presented stimulus was a GO/NO-GO stimulus, an Instructed stimulus, or novel (NEW) stimulus. Retrieval success related to recognition memory was isolated by contrasting activation from each stimulus set to a novel stimulus (i.e., an OLD > NEW contrast). To explore differences potentially related to source memory, separate contrasts were performed between stimulus sets. Results: No regions reached supralevel thresholds during the passive viewing task. However, a relatively similar set of regions was activated during active recognition regardless of the methods and included dorsolateral and ventrolateral prefrontal cortex, right inferior and posterior parietal regions and the occipitoparietal region, precuneus, lingual, fusiform gyri and cerebellum. Results also showed the magnitude of the functional response in the occipitoparietal region was inversely correlated with reaction times (RTs), such that the largest functional response and slowest RTs occurred to Instructed stimuli and the smallest functional response and fastest RTs occurred to GO stimuli, with effects to NO-GO stimuli intermediate. The inverse relation was also present bilaterally in the parahippocampus and hippocampus. Comparisons between stimulus sets also revealed regional differences potentially related to source memory. Conclusion: Recognition of stimuli previously associated with instructions and operant contingencies (i.e., discriminative stimuli) generally recruited similar inferior frontal and occipitoparietal regions and right posterior parietal cortex, with the right occipitoparietal region showing the largest effect. These findings suggest domain-general views of recognition memory may be applicable to understanding the neural correlates of control exerted by discriminative stimuli and suggest declarative memory processes are involved in human operant behavior. Page 1 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 and posterior parietal regions, including the precuneus, Background Numerous functional magnetic resonance imaging lingual gyrus, and particularly occipitoparietal regions (fMRI) studies on episodic and recognition memory for [12-16]. Findings highlighting a common spatially dis- words, picture and sounds, consistently find brain activa- tributed network during recognition memory of tion in various portions of the lateral and posterior pari- instructed and discriminative stimuli would facilitate the etal regions, medial and inferior frontal regions and generality of domain-general theories of human memory various medial temporal lobe structures [1-4]. The relia- functioning. Findings in line with our prediction would bility of findings has encouraged the development of also reinforce and extend nonhuman based neurophysio- domain-general views of human recognition memory [5- logical theories on the relation between operant behavior 7]. One common feature of many human neuroimaging and declarative memory, which involves the conscious studies is to give subjects verbal instructions to direct their recollection of facts and events [17-20]. attention to a specific stimulus attribute (e.g., perceptual, semantic, source, spatial), which then prompts encoding. In the present investigation, encoding of stimulus infor- Thus, instructions are a contextual variable that may be mation was prompted using three different methods prior manipulated to lay the foundation for subsequent mem- to neuroimaging. Encoding of two stimulus sets was ory formation. The question addressed in this investiga- prompted by operant contingencies embedded within a tion is whether the same or a similar neurophysiological GO/NO-GO task. Inclusion of the NO-GO condition, process is involved when the contextual variable prompt- which includes a contingency but no reward delivery, pro- ing memory formation involves contingency-shaped, vides a novel test of whether activation observed during rather than instructed responses. recognition of GO stimuli is reward dependent. Encoding of the third stimulus set was prompted by verbal instruc- Converging evidence from a diverse number of investiga- tions that emphasized memorizing stimuli. During two tions shows memory formation and subsequent recall/ separate functional neuroimaging runs, subjects com- recognition is highly sensitive to contextual variables pleted a passive and an active recognition memory task, present during encoding, particularly reward. For with task order counterbalanced across subjects. Both instance, Wittmann et al.  examined long-term recall tasks presented individual stimuli from each stimulus set for object pictures and reported greater dopaminergic and an additional novel stimulus ('NEW') used as a base- midbrain activation to items that predicted monetary line for the neuroimaging analysis. The passive memory rewards, reward associated items were recalled better, and task required only observation of stimuli. In contrast, the reward-associated items elicited greater hippocampal acti- active recognition memory task required making a source vation. Adcock et al.  has shown that that long-term or categorical judgment regarding whether a stimulus was memory for scenes encoded along with monetary reward a GO/NO-GO stimulus, an Instructed stimulus or a NEW enhanced recall and were associated with greater activa- stimulus. This methodology was adapted from episodic tion during encoding. Visual cortex and parietal regions memory studies in which encoded stimuli, referred to as associated with the allocation of spatial attention in a vis- 'OLD', are contrasted with 'NEW' stimuli to identify acti- ual cueing task also show enhancement by the presence of vation related to 'retrieval success.' Potential differences reward incentives for speeded performance . Ramnani related to source memory were examined by performing and Miall  also showed greater activation within the contrasts between stimulus sets. Finally, varying the left parahippocampal gyrus when reward was present in a response requirement (passive vs. active) between tasks motor task. enabled examination of the relation between regional activation and response dependency. This investigation examined the effects of three different methods of prompting encoding on activation during rec- Methods ognition memory. Encoding in one condition was Fifteen healthy, right-handed males (n = 8) and females prompted by verbal instructions. In the remaining condi- (n = 7) participated. Subjects were Johns Hopkins tions, encoding was prompted by trial and error learning employees, students, and Baltimore residents. All were within the context of an operant (instrumental) learning unfamiliar with the task and reported being between 18 task. We hypothesized that during operant learning, the and 50 years of age, right-handed, free of medications three-term contingency (i.e., stimulus-response-conse- affecting the central nervous system or the autonomic sys- quence relation) prompts encoding of a discriminative tem for at least 2 weeks, and without a personal history of stimulus in ways that parallel verbal instructions. Accord- psychiatric disorder or a psychiatric history in first-degree ingly, retrieval-based activation correlated with stimulus relatives. Informed, written consent was obtained from all recognition should be relatively similar between subjects according to the institutional guidelines estab- instructed stimuli and discriminative stimuli and be local- lished by the Johns Hopkins Human Subjects Protection ized in dorsolateral and ventrolateral prefrontal cortex Committee. Page 2 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 Experimental conditions Stimulus encoding occurred outside of the fMRI scanner approximately three hours before neuroimaging. Stimuli consisted of nine Greek letters (α, ∏, ∑, , μ, λ, δ, β, Ω), approximately 7.6 cm by 7.6 cm in size, that were ran- domly assigned to encoding conditions for each subject, thereby minimizing confounds related to stimulus fea- tures in the imaging analysis. Training took place in a quiet room with the subject seated in front of the compu- ter and keyboard. There were three encoding conditions: GO, NO-GO and Instructed. GO and NO-GO encoding conditions occurred concurrently during operant training. The order of completing encoding conditions was coun- terbalanced across subjects, such that half received the Instructed encoding condition first, followed by operant training under GO and NO-GO encoding conditions The sequence of extended operant training followed by BOLD functional MRI was modeled after established pro- cedures used in previous operant-fMRI investigations [for additional details see [21,22]]. At the start of training (i.e, encoding), task instructions emphasized that when a stimulus appeared on a computer screen pressing a desig- nated response button would sometimes produce money, thus, it was up to subjects to choose when to press/not to press, earn as much money as possible and to pay careful attention to the stimuli as they would be presented later Trial tional neuroima Figure 1 types used in each enco ging ding condition prior to func- during neuroimaging. Instructions highlighting the future Trial types used in each encoding condition prior to functional neuroimaging. (A) During GO trials, complet- memory test served the function of encouraging similar ing a response requirement on a response button in the levels of intentional encoding of stimulus information. presence of GO stimuli produced money. During NO-GO Operant training consisted of learning two stimulus- trials, withholding responding in the presence of NO-GO response-consequence contingencies: GO and NO-GO. stimuli for 10 s terminated the stimulus and trial. In the Three GO stimuli and three NO-GO stimuli were pre- Instructed encoding condition, subjects were told to memo- sented individually in a randomized order during training rize a set of stimuli. Subjects received equivalent amounts of (e.g., GO, GO, NO-GO, GO, NO-GO, etc...). Panel A exposure to stimuli in all three encoding conditions prior to labeled "Encoding Conditions" in Figure 1 provides a neuroimaging. (B) During the active recognition memory task schematic diagram for each contingency. For NO-GO completed during neuroimaging, stimuli from each encoding stimuli, a period of 10 s without a response in the pres- condition were presented in a random order along with a baseline stimulus (asterisk). The recognition response ence of the stimulus terminated the trial and initiated the involved making a categorical judgment regarding whether a next trial. For GO stimuli, reinforcers (either $0.05, $0.50 stimulus was observed in the GO/NO-GO training condition and $5.00) were delivered on a variable-ratio 3 reinforce- (button #1), the instructed condition (button #2), or was ment schedule for responding. After earning five consecu- NEW (button #3). tive reinforcers under a GO stimulus, the next stimulus in the order (GO or NO-GO) was presented. Total exposure to GO and NO-GO stimuli was found to not differ signif- icantly during encoding, thus differences in viewing dura- were instructed to memorize the stimuli over the next 6 tions between GO and NO-GO conditions would not minutes and to pay careful attention because the stimuli likely confound imaging results. Operant training contin- would be presented later during imaging – intentional ued until the total number of responses emitted in the encoding of stimulus information. A paired two-tailed t- presence of GO stimuli was greater than 90% of the total test was performed to determine whether differences number of responses emitted during a session – thus, per- existed in total duration of exposure to stimuli in the cent responses to NO-GO stimuli was less than 10% of the Instructed condition (group mean = 6 min (thus, SE = 0 total responses emitted. During the Instructed encoding s)) and discriminative stimuli (mean = 5 min 52 s (SE = 9 condition, three stimuli were printed on the computer s)). Results showed no significant differences in exposure screen for 6 min, as seen in Figure 1, panel A. Subjects (t (14) = 2.02, P = 0.06). Thus, exposure to stimuli com- Page 3 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 prising Instructed, GO and NO-GO encoding conditions fMRI analyses were similar, eliminating potential differences in viewing For a subject's imaging data to be included in the analysis, durations to stimuli during encoding as a potential con- head movement was limited to less than 2 mm. All pre- found in the imaging data. processing and data analysis were performed using statis- tical parametric mapping software, version 2 . EPI fMRI task and acquisition parameters images were slice-timing corrected to adjust for the lag Neuroimaging occurred approximately 2–3 hours after between slices during each TR, corrected for head motion training was completed. Subjects were placed in the scan- during scanning, and normalized to a standard template ner and handed a response box containing three response brain from the Montreal Neurological Institute (MNI) to buttons arranged vertically. Instructions described the get all participants into the same space . After normal- basic task and the function of each response button. Panel ization, voxels were resampled with a 2 × 2 × 2 mm voxel B in Figure 1 provides a schematic diagram of the recogni- size. EPI images were then spatially smoothed using a 6 tion memory task used and trial timings. Using an event mm full-width-half-maximum(FWHM) Gaussian kernel. related design, individual stimuli from each encoding High pass filtering was applied to the time series of EPI condition were randomly presented on 18 trials for 1500 images to remove the low frequency drift in EPI signal and ms followed by a blank screen averaging 4500 ms, which then subjected to a two-level analysis. At the first level, effectively 'jittered' stimulus presentations across time individual-subject models were constructed in which a such that stimulus onsets were separated by an average of linear regression analysis was performed between the 6 s. Subjects completed a passive and an active recognition observed event related EPI signals and onset times of stim- memory task, which were presented in a counterbalanced uli (GO, NO-GO, Instructed and NEW) . Contrast order across subjects. For the passive memory task, stimuli images were then produced by performing voxel-wise were presented and subjects were instructed to observe comparisons for stimuli within each encoding condition each stimulus and make no button presses. For the active (i.e., OLD) relative to the baseline stimulus (i.e., NEW). recognition memory task, subjects were instructed to press Contrast images were analyzed at the second 'random the button #1 (top button) if the stimulus was seen during effects' level using one-sample t-tests, for revealing the the behavioral (operant) training condition, button 2 main effect of recognition and condition-specific activa- (middle button) if the stimulus was seen during the tion, and multiple regression (simple correlation), for Instructed training condition, and button 3 (bottom but- revealing linear increases in activation across conditions ton) if the stimulus was novel (NEW). The NEW stimulus . The thresholds P < .001, uncorrected for multiple used was an asterisk and served as the baseline condition comparisons, and 20 contiguous voxels were used except for performing conventional OLD > NEW imaging con- where noted. Analyses of medial temporal regions were trasts to highlight regional activation correlated with rec- performed using separate anatomically defined masks, ognition memory. which employs a small volume correction, created with the Wake Forest University PickAtlas SPM2 plug-in . Functional MRI images were obtained on a 3 T Philips The location of voxels with significant activation was sum- MRI scanner. Eprime software controlled stimulus presen- marized by their local maxima separated by at least 8 mm, tation and recorded timing data. Task instructions and and by converting the maxima coordinates from MNI to stimuli were presented on a rear screen monitor viewed Talairach coordinate space using linear transformations through a mirror anchored to a standard head coil. After . These coordinates were finally assigned neuroana- an initial series of sagittal T1-weighted localizers, a set of tomic labels using human brain atlas' and the Talairach oblique T1-weighted images, angled parallel to the inter- Daemon . commissural line, were gathered. The fMRI data were acquired at the same slice locations. The T1 parameters Results were repetition time (TR) of 500 ms and an estimation Behavioral time (TE) of 11 ms. Functional MRI data were gathered All subjects responded with 100% accuracy during the using a single-shot echo planar imaging (EPI) sequence active recognition memory task. Paired t-test analyses for data acquisition, with a TR of 2000 ms, a TE of 50 ms, were used to compare differences in reaction times among and a 90-degree flip angle. The matrix size was 64 × 64 GO, NO-GO, Instructed and the NEW baseline condition. and the field of view 24 cm, yielding voxels measuring Group mean reaction times and standard deviations 3.75 × 3.75 mm in plane. Using these parameters, 43 con- appear in Figure 2. Reaction times for GO stimuli were tiguous slices were obtained angled parallel to the inter- found to be significantly faster than NO-GO ((t (14) = commissural line. 2.9, P = 0.0117) and Instructed stimuli (t (14) = 4.01, P = 0.0013), but not NEW stimuli (t (14) = .55, P = 0.591). All other comparisons did not reach significance, however, Page 4 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 regions that exceeded our thresholds during the passive viewing task. For the active recognition memory task, sub- sequent rows in Figure 3 (rows 2–4) highlight regional activation for each encoding condition relative to the NEW stimulus, with complete results summarized in Table 2. Across encoding conditions there was considera- ble overlap in the localization of activation, as well as notable magnitude effects – discussed below. Stimulus onsets elicited bilateral activation in posterior parietal regions centered near the occipitoparietal sulcus, with the effect larger in the right cerebrum. Moreover, activation was generally localized in inferior and middle/medial frontal regions and the right inferior and superior parietal cortex. Reac Figure 2 tion times during recognition memory Magnitude effect Reaction times during recognition memory. Group Given the orderly increases in reactions times observed mean reaction times and standard deviations of recognition across conditions (i.e., Instructed > NO-GO > GO) cou- memory judgments exhibited during neuroimaging to stimu- lus items with different encoding histories. Encoding pled with the observation of increases in the extent of acti- occurred prior to imaging and was prompted by three condi- vation across encoding conditions in Figure 3, we tions (1) GO stimulus items: pressing a button to earn performed a simple regression analysis to localize linear money under one set of stimuli; (2) NO-GO stimulus items: increases in activation across encoding conditions (i.e., inhibiting button pressing under a second set of stimuli; and Instructed > NO-GO > GO) with special attention given to (3) Instructed stimulus items: memorizing a third set of stim- occipitoparietal regions. The analysis used both P < .001 uli as prompted by verbal instructions. The item labeled and P < .000001 thresholds, uncorrected for multiple "NEW" was an asterisk presented during neuroimaging that comparisons, and an extent threshold of 20 contiguous prompted a button press and functioned as the baseline con- voxels. Results presented in Figure 3 (rows 5 and 6) and dition for assessing activation correlated with the onsets of Table 3 highlight regions showing significant increases in encoded stimulus items (i.e., OLD > NEW contrasts). Signifi- activation across encoding conditions. The primary find- cant differences in reaction times were observed between GO and NO-GO conditions and GO and Instructed condi- ing was activation centered near the occipitoparietal sul- tions. cus, with the extent of activation more extensive in the right cerebrum. Linear bilateral increases in activation were also observed in inferior and precentral frontal reaction times for NEW stimuli relative to Instructed stim- regions, cuneus, middle occipital gyrus and the superior uli did approach significance (t (14) = 1.97, P = 0.069). parietal region. Activation was also noted in the left medial frontal gyrus and right middle and superior gyrus, Neuroimaging lingual gyrus, precuneus and cerebellum. Results in Figure Main effect for recognition 3 also show at reduced statistical thresholds bilateral For the passive viewing task, voxel-wise comparisons increases in activation in the posterior parahippocampus revealed no regions that exceeded our thresholds. For the and hippocampus (parahippocampus: maxima = P < active recognition memory task, Figure 3 (row 1) and .001; left, t = 5.33, right t = 3.93). Plots of percent signal Table 1 present results for the main effect of recognition change for the hippocampus also highlight the linear memory (collapsed across encoding conditions) con- effect (left maxima at P = .011, t = 2.36, and right maxima trasted against activation to the NEW stimulus. Bilateral at P = .027, t = 1.97). activation was observed in inferior, middle, and superior frontal regions and posterior parietal regions that Source memory contrasts included the precuneus and cuneus localized near the Contrasts performed among the encoding conditions pro- occipitoparietal sulcus. Additional activation was noted in vides a means of exploring differences in activation during the left cingulate gyrus, medial frontal gyrus and fusiform recognition memory that might vary as a function of dif- gyrus and right lingual gyrus, middle occipital gyrus, infe- ferent methods or sources that prompted encoding of rior and superior parietal regions and cerebellum. stimulus information. Results highlighting voxel-wise dif- ferences between selected encoding conditions appear in Condition effects Table 4 (P < .005, uncorrected for multiple comparisons, Voxel-wise contrasts comparing stimuli within each using an extent threshold of 20 contiguous voxels). Con- encoding condition to the NEW stimulus revealed no trasting GO > Instructed revealed bilateral activation pri- Page 5 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 Table 1: Regional activation for main effect of recognition. Peak Region XY Z t BA Left Inferior Frontal Gyrus -30 21 -11 5.86 Medial Frontal Gyrus -4 29 37 4.68 6 Middle Frontal Gyrus -51 34 20 4.26 Superior Frontal Gyrus -20 59 6 5.78 Cingulate Gyrus -12 -55 29 5.82 31 Precuneus -24 -71 20 5.5 Cuneus -16 -64 9 6.18 Fusiform Gyrus -26 -55 -9 4.8 Right Inferior Frontal Gyrus 38 21 -3 6.07 Superior Frontal Gyrus 4 33 48 5.82 8 Middle Frontal Gyrus 50 16 40 4.52 8 Lingual Gyrus 16 -66 5 9.39 Precuneus 10 -71 26 8.76 Cuneus 4 -81 8 5 17 Middle Occipital Gyrus 40 -80 1 5.45 Inferior-Superior Parietal Lobule 32 -56 40 7.39 Declive 4 -76 -15 6.37 Medial Temporal Gyrus 46 -55 -2 5.96 marily in the insula and claustrum, regions with ties to involving operant contingencies. Each type of encoded affective processing and reward processing, as well as the stimulus set elicited bilateral activation near the occip- right cingulate and superior temporal gyrus. Contrasting itoparietal sulcus, with the effect larger in the right cere- NO-GO > Instructed evidenced greater bilateral activation brum. Moreover, activation was observed in inferior and in the supramarginal gyrus and parahippocampus and the middle/medial frontal regions and the right inferior and left precentral gyrus and insula and right superior and superior parietal cortex. Third, the magnitude of the func- medial frontal gyrus, cingulate and fusiform gyrus. For the tional response in the occipitoparietal region was also GO > NO-GO contrast, GO stimuli elicited activation in found to be inversely correlated with reaction times (RTs), the precuneus. Contrasting NO-GO > GO revealed bilat- such that the largest functional response and slowest RTs eral activation in middle frontal and precentral cortices, occurred to Instructed stimuli and the smallest functional cingulate, lateral posterior nucleus of the thalamus, fusi- response and fastest RTs occurred to GO stimuli, with form gyrus and precuneus. Right localized activation effects to NO-GO stimuli intermediate. The inverse rela- occurred in the medial, superior and postcentral frontal tion was also present bilaterally in the parahippocampus gyri, supramarginal and angular gyri and the inferior pari- and hippocampus. Linear bilateral increases in activation etal lobule. Regional activation was also observed in the were also observed in inferior and precentral frontal left posterior cingulate, insula and inferior temporal regions, cuneus, middle occipital and the superior parietal gyrus. region. Differences in the localization of activation between con- Discussion In summary, the present investigation yielded three major ditions and the linear increases in activation across condi- findings of importance to human neuroimaging investi- tions suggests the methods used to direct attention and gations on memory and human operant behavior. First, prompt encoding of stimulus information may modulate voxel-wise contrasts revealed no regions that reached sta- activation during recognition. Several prior investigations tistical significance during the passive viewing task, which have shown that elaborating on stimulus meaning during suggests simple presentations of OLD stimuli is not suffi- encoding facilitates subsequent recognition and retrieval. cient to elicit significant activation. However, activation This "levels of processing" view suggests that stimuli during active recognition was present bilaterally in infe- encoded under operant contingencies may be more elab- rior, middle, and superior frontal regions and posterior orately (deeply) processed because of the demands associ- parietal regions that included the precuenus and cuneus ated with trial and error learning, that is, forming the localized near the occipitoparietal sulcus. Second, the relations among the stimulus, response and the conse- localization of activation during recognition memory was quence. Accordingly, discriminative stimuli might be found to be relatively similar for stimuli encoded under expected to be easily recognized and, therefore, be associ- conditions involving verbal instructions and conditions ated with faster reaction times and greater activation com- Page 6 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 pared to stimuli encoded under instructions, which presumably may be processed on a more superficial level (shallow encoding) [e.g., ]. Naturally, this fundamen- tal idea may not be limited to tasks involving operant con- tingencies, but rather extend to conditions that require extensive interactions with stimuli. However, while the level of processing idea is consistent with our observation of significantly faster reaction times for GO and NO-GO stimuli relative to Instructed stimuli, this view does not account for our findings that showed greater activation for Instructed stimuli relative to GO an NO-GO stimuli, par- ticularly in the occipitoparietal region. An alternative account suggested by findings from verbal working memory studies, in which slow reaction times were accompanied by a large functional response in pos- terior parietal cortex, is that recognition of Instructed stimuli was relatively more 'difficult' [14,15]. Related to the present findings, the slower reactions times to Instructed stimuli, and the larger functional response sug- gests these effects were a function of either differences in the methods that prompted encoding (instructed versus contingency shaped) or some other aspect of our proce- dure. Since the order of exposure to conditions was coun- terbalanced across subjects and the duration of exposure to stimuli across conditions was similar, the linear magni- tude effect seems unrelated to these factors. One proce- dural difference that may have influenced the linear magnitude effect was presenting Instructed stimuli as a group and presenting discriminative stimuli individually. However, it is difficult to develop a plausible account of how differences in presentation would produce the linear increases observed. It seems more likely that once the operant contingencies (GO or NO-GO) exerted firm con- trol over behavior, recognition required fewer resources, which resulted in less activation. By comparison, encod- ing of stimulus information prompted by verbal instruc- A Figure 3 ctivation correlated with recognition memory by condition tions required much less behavioral involvement. These Activation correlated with recognition memory by differences in behavioral control or involvement pro- condition. The top row shows regional activation for the duced by either operant contingencies or simply task main effect of recognition relative to baseline (i.e, the NEW involvement may be responsible for the magnitude effect stimulus). Subsequent rows reveal regional activation during observed. Accordingly, this view predicts greater levels of recognition of GO, NO-GO and Instructed (INS) stimulus behavioral control or involvement prompted by a proce- items relative to a baseline. The most prominent and consist- dure would result in easier recognition, faster reaction ently activated region across conditions was the occipitopari- times, and less activation in the occipitoparietal region. etal region. Activation was also noted in varying degrees in dorsolateral and ventrolateral prefrontal cortex and poste- Collectively, the present findings support our prediction rior parietal regions. Linear increases in activation reflecting that during operant or instrumental learning, the operant magnitude differences across conditions were also noted (Instructed > NO-GO > GO). The regional increases were contingencies functioned in much the same way as verbal centered in the precuneus, superior and inferior frontal gyrus instructions by eliciting a relatively similar set of 'retrieval and right superior parietal regions (results shown in panel A. success' regions, with the largest effects observed in the at P < .001 and in panel B. at P < .000001). The insert shows occipitoparietal region. These results provide some pre- bilateral increases in the posterior parahippocampus and hip- liminary support for extending domain-general theories pocampus. of human recognition memory, based largely on pictures, words and sounds, and encoding prompted by verbal Page 7 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 Table 2: Regional activation during recognition for each encoding condition. Peak Contrast and Region X Y Z t BA GO > NEW Left Inferior Frontal Gyrus -36 17 -6 4.74 47 Cingulate Gyrus -10 -53 27 4.44 Precuneus -22 -73 20 5.88 31 Cuneus -20 -86 25 4.61 18 Cuneus -14 -64 9 4.51 Right Medial Frontal Gyrus 36 30 19 5.16 Posterior Cingulate 8 -67 11 5.36 30 Cuneus 10 -76 26 6.97 18 Middle Occipital Gyrus 40 -78 1 5.24 Lingual Gyrus 14 -66 -2 4.67 18 Medial Temporal Gyrus 36 -63 29 5.18 NO-GO > NEW Left Middle Frontal Gyrus -51 34 20 5.50 Medial Frontal Gyrus -6 44 16 5.23 9 Inferior Frontal Gyrus -32 25 -3 4.98 Parahippocampus -26 -45 -10 6.89 37 Precuneus 0 -72 29 6.16 Fusiform Gyrus -26 -53 -7 5.00 Cuneus -24 -82 24 4.90 Tonsil -12 -48 -31 7.40 Culmen -2 -55 -16 4.36 Right Inferior Frontal Gyrus 38 32 15 7.87 Superior Frontal Gyrus 2 14 56 5.51 Middle Frontal Gyrus 48 8 36 5.47 9 Medial Frontal Gyrus 2 20 45 4.48 Precentral Gyrus 53 10 12 4.56 44 Frontal-Temporal 55 12 3 4.65 Lingual Gyrus 16 -66 5 8.65 Precuneus 10 -73 26 8.47 Cuneus 26 -74 31 4.46 Inferior Parietal Lobule 36 -54 38 6.36 Fusiform Gyrus 48 -57 -12 6.72 37 Medial Temporal Gyrus 34 -61 27 6.01 Superior Temporal Gyrus 44 -53 25 5.37 39 Instructed > NEW Left Inferior Frontal Gyrus -36 29 4 7.72 Middle Frontal Gyrus -50 17 34 5.72 Posterior Cingulate -16 -60 10 5.56 Middle Occipital Gyrus -48 -65 -10 5.88 37 Cuneus -24 -82 26 5.12 Lingual -12 -49 1 4.56 19 Superior Parietal Lobule -36 -60 49 5.71 Inferior Parietal Lobule -36 -58 42 4.18 Declive -6 -76 -15 4.05 Uvula -30 -65 -25 4.27 Insula -40 19 0 4.89 13 Medial Temporal Gyrus -36 -77 19 5.11 Right Inferior Frontal Gyrus 53 12 12 5.88 44 Middle Frontal Gyrus 50 6 37 5.64 9 Medial Frontal Gyrus 6 16 47 5.43 6 Cingulate Gyrus 8 23 39 4.26 Cuneus 6 -80 32 8.22 19 Page 8 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 Table 2: Regional activation during recognition for each encoding condition. (Continued) Lingual Gyrus 16 -62 0 7.57 19 Middle Occipital Gyrus 48 -74 -3 5.61 Inferior Parietal Lobule 32 -56 43 9.21 Superior Parietal Lobule 34 -64 44 5.00 7 Declive 28 -63 -17 7.60 Uvula 34 -63 -25 4.62 Pyramis 10 -75 -27 6.44 Insula 38 21 1 4.93 Fusiform Gyrus 50 -41 -11 4.55 37 instructions [5-7], to stimuli encoded through nonverbal, etal region, but the magnitude of the functional response goal-directed experiences involving operant learning was modulated by conditions present during encoding. In processes. Because recognition memory is considered a general, the present findings suggest domain-general declarative memory process requiring conscious recollec- views regarding the neural correlates of recognition mem- tion of stimulus information, the observation of similar ory may be relevant to understanding operant behavior activation patterns to Instructed and discriminative stim- and offer additional support for operant learning as uli suggests similar neural process are engaged during involving declarative memory. At a broader level, neu- memory retrieval and situations involving discriminative roimaging investigations on human memory systems that stimulus control. employ both conventional human imaging research pro- cedures (i.e., instructed encoding) and nonhuman research procedures (i.e. operant learning paradigms) Conclusion Our investigation examined activation during recognition provide a novel context in which to investigate cross-spe- memory to nonverbal stimuli previously encoded under cies functional-anatomical similarities. operant learning contingencies and nonverbal stimuli encoded under verbal instructions. Results showed a rela- Competing interests tively similar spatially distributed network was activated The author(s) declare that they have no competing inter- during active recognition, especially in the occipitopari- ests. Table 3: Linear increases in activation: Instructed > NO-GO > GO. Peak Region X Y Z t BA Left Inferior Frontal Gyrus -34 27 4 7.82 Medial Frontal Gyrus -4 27 37 6.00 Precentral Gyrus -42 25 34 6.27 9 Cuneus -24 -80 24 7.28 Middle Occipital Gyrus -18 -87 15 6.36 18 Superior Parietal Lobule -32 -70 46 6.23 Right Medial Frontal Gyrus 40 32 17 7.29 Inferior Frontal Gyrus 38 21 -3 7.12 Middle Frontal Gyrus 50 8 38 6.89 Precentral Gyrus 42 1 26 6.85 6 Superior Frontal Gyrus 4 14 56 6.28 6 Lingual Gyrus 16 -66 5 10.49 Cuneus 8 -68 7 8.20 Precuneus 10 -71 26 9.35 Cuneus 8 -78 24 9.33 Middle Occipital Gyrus 34 -81 21 6.52 19 Superior Parietal Lobule 36 -62 44 6.26 7 Precuneus 32 -66 35 6.24 Declive 4 -76 -15 7.19 Pyramis 10 -75 -23 6.62 Inferior Temporal Gyrus 46 -58 -2 7.31 Page 9 of 11 (page number not for citation purposes) Behavioral and Brain Functions 2007, 3:44 http://www.behavioralandbrainfunctions.com/content/3/1/44 Table 4: Regional activation for contrasts between encoding conditions. Peak Contrast and Region X Y Z t BA GO > Instructed Left Insula -42 -19 5 5.28 13 Claustrum -34 -15 6 4.38 Right Insula 32 -24 21 6.91 Cingulate 8 -10 36 4.88 Superior Temporal Gyrus 48 -42 15 4.51 Precuneus 22 -51 30 4.13 GO > NO-GO Right Precuneus 20 -57 32 3.75 NO-GO > Instructed Left Precentral Gyrus -44 -6 26 3.49 Parahippocampus -22 -17 -23 4.5 Insula -28 -32 18 5.6 Supramarginal Gyrus -44 -49 30 4.34 Right Superior Frontal Gyrus 10 56 32 4.07 9 Medial Frontal Gyrus 10 48 34 3.32 Cingulate 8 -41 33 5.59 Parahippocampus 38 -43 -6 3.41 Fusiform Gyrus 34 -41 -13 4.58 Supramarginal Gyrus 46 -53 27 3.46 NO-GO > GO Left Middle Frontal Gyrus -46 12 38 4.22 8 Precentral Gyrus -42 17 34 3.56 9 Cingulate -8 12 38 3.92 Posterior Cingulate -4 -38 24 3.24 23 Thalamus: Lat Post Nuc. -20 -21 14 4.51 Insula -32 -28 16 3.70 13 Inferior Temporal Gyrus -48 -66 -2 5.54 Fusiform Gyrus -44 -49 -16 3.94 Precuneus -12 -48 47 4.51 7 Right Medial Frontal Gyrus 8 29 43 6.48 8 Middle Frontal Gyrus 26 16 42 6.83 Precentral Gyrus 48 1 26 5.10 6 Superior Frontal Gyrus 24 48 23 4.71 Thalamus: Lat Post Nuc. 20 -19 16 5.26 Cingulate 14 9 35 6.20 32 Fusiform Gyrus 50 -45 -15 4.28 37 Supramarginal Gyrus 46 -37 33 5.39 Angular Gyrus 40 -55 34 4.55 Inferior Parietal Lobule 42 -52 43 4.50 40 Precuneus 8 -62 38 4.01 7 Postcentral Gyrus 40 -29 51 3.56 Authors' contributions References 1. 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