Monkey Inferior Temporal Cortex Research Articles

Surgical Procedure for Implantation of Opto-Array in Nonhuman Primates.

Optogenetics allows precise temporal control of neuronal activity in the brain. Engineered viral vectors are routinely used to transduce neurons with light-sensitive opsins. However, reliable virus injection and light delivery in animals with large brains, such as nonhuman primates, has proven challenging. The Opto-Array is a novel yet simple device that is used to deliver light to extended regions of the cortex surface for high-throughput behavioral optogenetics in large brains. Here we present protocols for surgical delivery of virus (Basic Protocol 1) and implantation of the Opto-Array (Basic Protocol 2) in two separate surgeries in a rhesus monkey's inferior temporal cortex. As a proof of concept, we measured the behavioral performance of an animal detecting cortical optogenetic stimulations (Basic Protocol 3) with different illumination power and duration using the Opto-Array. The animal was able to detect the optogenetic stimulation for all tested illumination powers and durations. Regression analysis also showed both power and duration of illumination significantly modulate the detectability of the optogenetic stimulation. The outcome of this approach is superior to the standard practice of injecting and recording through a chamber for large areas of the cortex surface. Moreover, the chronic nature of the Opto-Array allows perturbation of neuronal activity of the same site across multiple sessions because it is highly stable; thus, data can be pooled over months. The detailed surgical method presented here makes it possible to use optogenetics to modulate neuronal activity across large regions of the cortex surface in the nonhuman primate brain. This method also lays the groundwork for future attempts to use optogenetics to restore vision in humans. © 2023 The Authors. Current Protocols published by Wiley Periodicals LLC. Basic Protocol 1: Virus injection surgery Basic Protocol 2: Opto-Array implantation surgery Basic Protocol 3: Cortical Perturbation Detection (CPD) task behavioral training.

A separable neural code in monkey IT enables perfect CAPTCHA decoding.

Reading distorted letters is easy for us but so challenging for the machine vision that it is used on websites as CAPTCHA (Completely Automated Public Turing Test to tell Computers and Humans Apart). How does our brain solve this problem? One solution is to have neurons selective for letter combinations but invariant to distortions. Another is for neurons to encode letter distortions and longer strings to enable separable decoding. Here, we provide evidence for the latter possibility using neural recordings in the monkey inferior temporal (IT) cortex. Neural responses to distorted strings were explained better as a product (but not sum) of shape and distortion tuning, whereas by contrast, responses to letter combinations were explained better as a sum (but not product) of letters. These two rules were sufficient for perfect CAPTCHA decoding and were also emergent in neural networks trained for word recognition. Thus, a separable neural code enables efficient letter recognition.NEW & NOTEWORTHY Many websites ask us to recognize distorted letters to deny access to malicious computer programs. Why is this task easy for our brains but hard for the computers? Here, we show that, in the monkey inferior temporal cortex, an area critical for recognition, single neurons encode distorted letter strings according to highly systematic rules that enable perfect distorted letter decoding. Remarkably, the same rules were present in neural networks trained for text recognition.

Face Repetition Probability Does Not Affect Repetition Suppression in Macaque Inferotemporal Cortex.

Repetition suppression, which refers to reduced neural activity for repeated stimuli, is typically explained by bottom-up or local adaptation mechanisms. However, recent theories have emphasized the role of top-down processes, suggesting that this response reduction reflects the fulfillment of perceptual expectations. To support this, an influential human fMRI study showed that the magnitude of suppression is modulated by the probability of a repetition. No such repetition probability effect was found in macaque inferior temporal (IT) cortex for spiking activity despite the presence of repetition suppression. Contrary to the human fMRI studies that showed an effect of repetition probability, the macaque single-unit study used a large variety of unfamiliar stimuli and the monkeys were not required to attend the stimuli. Here, as in the human fMRI studies, we used faces as stimuli and made the monkeys attend to the stimulus content. We simultaneously recorded spiking activity and local field potentials (LFPs) in the middle lateral face patch (ML) of one monkey (male) and a face-responsive region of another (female). Although we observed significant repetition suppression of spiking activity and high gamma-band LFPs in both animals, there were no effects of repetition probability even when repetitions were task relevant and repetition probability affected behavioral decisions. In conclusion, despite the use of face stimuli and a stimulus-related task, no neural signature of repetition probability was present for faces in a face responsive patch of macaque IT. This further challenges a general perceptual expectation account of repetition suppression.SIGNIFICANCE STATEMENT Repetition suppression is a reduced brain activity for repeated stimuli commonly observed across species. In the predictive coding framework, such suppression is thought to reflect fulfilled perceptual expectations. Although this hypothesis is supported by several human fMRI studies reporting an effect of repetition probability on repetition suppression, this could not be replicated in single-cell recordings in monkey inferior temporal (IT) cortex. Subsequent studies narrowed down the conditions for the effect to requiring attention and being limited to particular stimulus categories such as faces. Here, we show that, even under these conditions, repetition suppression in monkey IT neurons is still unaffected by repetition probability, even in a task with a behavioral effect, challenging the perceptual expectation account of repetition suppression.

Categorization in monkey inferior temporal cortex determined by image features, not acquired knowledge

Categorization in monkey inferior temporal cortex determined by image features, not acquired knowledge

Low dimensional representation of face space by face-selective inferior temporal neurons.

The representation of visual objects in primate brain is distributed and multiple neurons are involved in encoding each object. One way to understand the neural basis of object representation is to estimate the number of neural dimensions that are needed for veridical representation of object categories. In this study, the characteristics of the match between physical-shape and neural representational spaces in monkey inferior temporal (IT) cortex were evaluated. Specifically, we examined how the number of neural dimensions, stimulus behavioral saliency and stimulus category selectivity of neurons affected the correlation between shape and neural representational spaces in IT cortex. Single-unit recordings from monkey IT cortex revealed that there was a significant match between face space and its neural representation at lower neural dimensions, whereas the optimal match for the non-face objects was observed at higher neural dimensions. There was a statistically significant match between the face and neural spaces only in the face-selective neurons, whereas a significant match was observed for non-face objects in all neurons regardless of their category selectivity. Interestingly, the face neurons showed a higher match for the non-face objects than for the faces at higher neural dimensions. The optimal representation of face space in the responses of the face neurons was a low dimensional map that emerged early (~150ms post-stimulus onset) and was followed by a high dimensional and relatively late (~300ms) map for the non-face stimuli. These results support a multiplexing function for the face neurons in the representation of very similar shape spaces, but with different dimensionality and timing scales.

Neurophysiological Organization of the Middle Face Patch in Macaque Inferior Temporal Cortex.

The underlying organization of neurons that give rise to the large spatial regions of activity observed with fMRI is not well understood. Neurophysiological studies that have targeted the fMRI identified face patches in monkeys have provided evidence for both large-scale clustering and a heterogeneous spatial organization. Here we used a novel x-ray imaging system to spatially map the responses of hundreds of sites in and around the middle face patch. We observed that face-selective signal localized to the middle face patch was characterized by a gradual spatial enrichment. Furthermore, strongly face-selective sites were ∼40 times more likely to be found inside the patch than outside of the patch.

Seeing a straight line on a curved surface: decoupling of patterns from surfaces by single IT neurons.

We have no difficulty seeing a straight line on a curved piece of paper, but in fact, doing so requires decoupling the shape of the surface from the pattern itself. Here we report a novel form of invariance in the visual cortex: single neurons in monkey inferior temporal cortex respond similarly to congruent transformations of patterns and surfaces, in effect decoupling patterns from the surface on which they are overlaid.

Grandmother cells: much ado about nothing

ABSTRACTWe do not dispute the possibility of the existence in the brain of “grandmother cells”, which are very finely tuned neurons that fire only in the presence of specific objects or categories. However, we question the causal efficacy of such neurons at the functional or behaviour level. We claim that, even though very familiar items, such as “my grandmother”, may well have associated grandmother neurons, these neurons have very little, or no impact on the actual recognition of my grandmother. A study by Thomas, Van Hulle, and Vogels [(2002). Encoding of categories by noncategory-specific neurons in the inferior temporal cortex. Journal of Cognitive Neuroscience, 13, 190–200. doi:10.1162/089892901564252] found finely tuned, category-specific neurons in the inferior temporal cortex of monkeys, but also found that when these neurons were removed from their analysis, this had no effect on categorisation performance. Further, we have found no reported cases of the loss of recognition of single, highly familiar objects, which also argues for a lack of causal efficacy of grandmother-cell neurons.

The impact of orientation filtering on face-selective neurons in monkey inferior temporal cortex.

Faces convey complex social signals to primates. These signals are tolerant of some image transformations (e.g. changes in size) but not others (e.g. picture-plane rotation). By filtering face stimuli for orientation content, studies of human behavior and brain responses have shown that face processing is tuned to selective orientation ranges. In the present study, for the first time, we recorded the responses of face-selective neurons in monkey inferior temporal (IT) cortex to intact and scrambled faces that were filtered to selectively preserve horizontal or vertical information. Guided by functional maps, we recorded neurons in the lateral middle patch (ML), the lateral anterior patch (AL), and an additional region located outside of the functionally defined face-patches (CONTROL). We found that neurons in ML preferred horizontal-passed faces over their vertical-passed counterparts. Neurons in AL, however, had a preference for vertical-passed faces, while neurons in CONTROL had no systematic preference. Importantly, orientation filtering did not modulate the firing rate of neurons to phase-scrambled face stimuli in any recording region. Together these results suggest that face-selective neurons found in the face-selective patches are differentially tuned to orientation content, with horizontal tuning in area ML and vertical tuning in area AL.

Simple Learned Weighted Sums of Inferior Temporal Neuronal Firing Rates Accurately Predict Human Core Object Recognition Performance.

To go beyond qualitative models of the biological substrate of object recognition, we ask: can a single ventral stream neuronal linking hypothesis quantitatively account for core object recognition performance over a broad range of tasks? We measured human performance in 64 object recognition tests using thousands of challenging images that explore shape similarity and identity preserving object variation. We then used multielectrode arrays to measure neuronal population responses to those same images in visual areas V4 and inferior temporal (IT) cortex of monkeys and simulated V1 population responses. We tested leading candidate linking hypotheses and control hypotheses, each postulating how ventral stream neuronal responses underlie object recognition behavior. Specifically, for each hypothesis, we computed the predicted performance on the 64 tests and compared it with the measured pattern of human performance. All tested hypotheses based on low- and mid-level visually evoked activity (pixels, V1, and V4) were very poor predictors of the human behavioral pattern. However, simple learned weighted sums of distributed average IT firing rates exactly predicted the behavioral pattern. More elaborate linking hypotheses relying on IT trial-by-trial correlational structure, finer IT temporal codes, or ones that strictly respect the known spatial substructures of IT ("face patches") did not improve predictive power. Although these results do not reject those more elaborate hypotheses, they suggest a simple, sufficient quantitative model: each object recognition task is learned from the spatially distributed mean firing rates (100 ms) of ∼60,000 IT neurons and is executed as a simple weighted sum of those firing rates. Significance statement: We sought to go beyond qualitative models of visual object recognition and determine whether a single neuronal linking hypothesis can quantitatively account for core object recognition behavior. To achieve this, we designed a database of images for evaluating object recognition performance. We used multielectrode arrays to characterize hundreds of neurons in the visual ventral stream of nonhuman primates and measured the object recognition performance of >100 human observers. Remarkably, we found that simple learned weighted sums of firing rates of neurons in monkey inferior temporal (IT) cortex accurately predicted human performance. Although previous work led us to expect that IT would outperform V4, we were surprised by the quantitative precision with which simple IT-based linking hypotheses accounted for human behavior.

Neural Correlate of the Thatcher Face Illusion in a Monkey Face-Selective Patch.

Compelling evidence that our sensitivity to facial structure is conserved across the primate order comes from studies of the "Thatcher face illusion": humans and monkeys notice changes in the orientation of facial features (e.g., the eyes) only when faces are upright, not when faces are upside down. Although it is presumed that face perception in primates depends on face-selective neurons in the inferior temporal (IT) cortex, it is not known whether these neurons respond differentially to upright faces with inverted features. Using microelectrodes guided by functional MRI mapping, we recorded cell responses in three regions of monkey IT cortex. We report an interaction in the middle lateral face patch (ML) between the global orientation of a face and the local orientation of its eyes, a response profile consistent with the perception of the Thatcher illusion. This increased sensitivity to eye orientation in upright faces resisted changes in screen location and was not found among face-selective neurons in other areas of IT cortex, including neurons in another face-selective region, the anterior lateral face patch. We conclude that the Thatcher face illusion is correlated with a pattern of activity in the ML that encodes faces according to a flexible holistic template.

Neural correlates of statistical learning in the inferior-temporal cortex of rhesus monkeys.

Event Abstract Back to Event Neural correlates of statistical learning in the inferior-temporal cortex of rhesus monkeys. Peter Kaposvari1*, Susheel Kumar1 and Rufin Vogels1 1 KU Leuven, Laboratorium Neuro - en Psychofysiologie, Belgium We learn to implicitly extract the statistical regularities in the environment around us, e.g. sequences of stimuli that follow each other (e.g. letters in specific words). In the visual domain, human observers can extract regular sequences of visual stimuli from a continuous stream of visual shapes. The neural correlates of such visual sequence learning are still unclear. Here, we determined whether a neural correlate of short sequences of visual images, presented in a continuous stream, is present in macaque inferior temporal (IT) cortex. Two monkeys passively fixated while a continuous stream of 3 fixed sequences of 5 grayscale images of animals of various species each were presented in a random order. After a passive exposure of two months, we assessed whether the responses of IT neurons showed a correlate of the sequences by introducing deviant stimuli in the fixed standard sets. We compared the multiunit neuronal responses for the deviant stimuli with identical stimuli when presented in the standard, learned sequence. We observed a significant enhancement of the responses to the deviant stimulus and the trailing standard stimuli, when the deviant was either from the same sequence (p <0.05 for each monkey) or from the other two sequences (p <0.05 for each monkey). The neuronal responses to a second deviant stimulus (which followed the first deviant in the standard set) did not differ significantly from the standard. These results demonstrate that monkey IT cortex encodes at least part of a learned temporal sequence in which a stimulus is presented. Acknowledgements This work was supported by Fonds voor Wetenschappelijk Onderzoek Vlaanderen (G.0582.12N), Interuniversitaire Attractiepool, Programma Financiering (PF 10/008), European Community’s Seventh Framework Programme FP7/2007-2013 under grant agreement number PITN-GA-2008-290011 and Odysseus grant (G.007.12N). Keywords: sequence learning, statistical learning, rhesus macaque, Inferotemporal cortex, single-unit Conference: 11th National Congress of the Belgian Society for Neuroscience, Mons, Belgium, 22 May - 22 May, 2015. Presentation Type: Poster presentation Topic: Neuroscience Citation: Kaposvari P, Kumar S and Vogels R (2015). Neural correlates of statistical learning in the inferior-temporal cortex of rhesus monkeys.. Front. Neurosci. Conference Abstract: 11th National Congress of the Belgian Society for Neuroscience. doi: 10.3389/conf.fnins.2015.89.00063 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 30 Apr 2015; Published Online: 05 May 2015. * Correspondence: PhD. Peter Kaposvari, KU Leuven, Laboratorium Neuro - en Psychofysiologie, Leuven, 3000, Belgium, Peter.Kaposvari@med.kuleuven.be Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Peter Kaposvari Susheel Kumar Rufin Vogels Google Peter Kaposvari Susheel Kumar Rufin Vogels Google Scholar Peter Kaposvari Susheel Kumar Rufin Vogels PubMed Peter Kaposvari Susheel Kumar Rufin Vogels Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

High baseline activity in inferior temporal cortex improves neural and behavioral discriminability during visual categorization.

Spontaneous firing is a ubiquitous property of neural activity in the brain. Recent literature suggests that this baseline activity plays a key role in perception. However, it is not known how the baseline activity contributes to neural coding and behavior. Here, by recording from the single neurons in the inferior temporal cortex of monkeys performing a visual categorization task, we thoroughly explored the relationship between baseline activity, the evoked response, and behavior. Specifically we found that a low-frequency (<8 Hz) oscillation in the spike train, prior and phase-locked to the stimulus onset, was correlated with increased gamma power and neuronal baseline activity. This enhancement of the baseline activity was then followed by an increase in the neural selectivity and the response reliability and eventually a higher behavioral performance.

Perceptual gloss parameters are encoded by population responses in the monkey inferior temporal cortex.

There are neurons localized in the lower bank of the superior temporal sulcus (STS) in the inferior temporal (IT) cortex of the monkey that selectively respond to specific ranges of gloss characterized by combinations of three physical reflectance parameters: specular reflectance (ρs), diffuse reflectance (ρd), and spread of specular reflection (α; Nishio et al., 2012). In the present study, we examined how the activities of these gloss-selective IT neurons are related to perceived gloss. In an earlier psychophysical study, Ferwerda et al. (2001) identified a perceptually uniform gloss space defined by two axes where the c-axis corresponds to a nonlinear combination of ρs and ρd and the d-axis corresponds to 1 - α. In the present study, we tested the responses of gloss-selective neurons to stimuli in the perceptual gloss space defined by the c- and d-axes. We found that gloss-selective neurons systematically changed their responses in the perceptual gloss space, and the distribution of the tuning directions of the population of gloss-selective neurons is biased toward directions in which perceived gloss increases. We also found that a set of perceptual gloss parameters as well as surface albedo can be well explained by the population activities of gloss-selective neurons, and that these parameters are likely encoded by the gloss-selective neurons in this area of the STS to represent various glosses. These results thus provide evidence that the IT cortex represents perceptual gloss space.

Fine-grained stimulus representations in body selective areas of human occipito-temporal cortex

Neurophysiological and functional imaging studies have investigated the representation of animate and inanimate stimulus classes in monkey inferior temporal (IT) and human occipito-temporal cortex (OTC). These studies proposed a distributed representation of stimulus categories across IT and OTC and at the same time highlighted category specific modules for the processing of bodies, faces and objects. Here, we investigated whether the stimulus representation within the extrastriate (EBA) and the fusiform (FBA) body areas differed from the representation across OTC. To address this question, we performed an event-related fMRI experiment, evaluating the pattern of activation elicited by 200 individual stimuli that had already been extensively tested in our earlier monkey imaging and single cell studies (Popivanov et al., 2012, 2014). The set contained achromatic images of headless monkey and human bodies, two sets of man-made objects, monkey and human faces, four-legged mammals, birds, fruits, and sculptures. The fMRI response patterns within EBA and FBA primarily distinguished bodies from non-body stimuli, with subtle differences between the areas. However, despite responding on average stronger to bodies than to other categories, classification performance for preferred and non-preferred categories was comparable. OTC primarily distinguished animate from inanimate stimuli. However, cluster analysis revealed a much more fine-grained representation with several homogeneous clusters consisting entirely of stimuli of individual categories. Overall, our data suggest that category representation varies with location within OTC. Nevertheless, body modules contain information to discriminate also non-preferred stimuli and show an increasing specificity in a posterior to anterior gradient.

Coarse orientation discrimination is impaired by microstimulation of macaque posterior inferior temporal cortex.

Event Abstract Back to Event Coarse orientation discrimination is impaired by microstimulation of macaque posterior inferior temporal cortex. Hamed Zivari Adab1 and RUFIN VOGELS1* 1 KU Leuven, KU Leuven Medical School, Belgium We have recently identified an orientation selective region in the posterior inferior temporal (PIT) cortex of monkeys with response properties that are affected by practicing a coarse orientation discrimination task (Adab et al., 2014). In this task, subjects discriminate two orthogonal gratings that are masked by noise (variable signal to noise ratio; SNR). To assess whether there is a causal link between PIT activity and the monkey’s decision, we applied microstimulation in PIT while the monkeys were performing the coarse orientation and a control, color discrimination task. In the latter task the noisy gratings were presented at the same location as in the orientation task but were irrelevant for the task performance. The color patch was presented ipsilateral to the stimulated hemisphere at 10.3 deg eccentricity. Microstimulation consisted of bipolar, cathodal phase first, current pulses of 650 uA delivered at 300 Hz. Each pulse was 0.25 ms in duration with 0.01 ms between the cathodal and anodal phase. Stimulating pulses were delivered for 250 ms (equal to grating duration) with a 50 ms delay following onset of the grating. The stimulation (50% of the total number of trials) and no-stimulation trials were randomly interleaved. Percent correct performance as a function of SNR in the orientation discrimination task was fitted with a cumulative normal function for stimulation and no-stimulation conditions, separately, estimating 75% correct thresholds. Microstimulation of PIT increased the thresholds dramatically (median percent threshold increase: Monkey M: 195%, monkey P: 281%). The behavioral impairment was also obtained with currents as low as 100 uA. Microstimulation after the stimulus presentation but before the saccadic response had no effect. Performance in the color discrimination task was affected but less so (median percent decrease in z-transformed percent correct: monkey M: 6%, monkey P: 9%), suggesting that the microstimulation effect is specific for the properties of the discrimination task. To test for visual area specificity, we microstimulated 3 regions 6 mm anterior to PIT of monkey P: the upper bank of the superior temporal sulcus (USTS), the lower bank of the STS (LSTS) and the lateral convexity of inferotemporal (LCIT) cortex. Whereas no significant effect of stimulation on the threshold in orientation discrimination was found in the USTS (median: 1.7%), significant but only moderate to weak effects were present in the LSTS (median: 139%) and LCIT (median: 40%). Overall, these data support the hypothesis that PIT is the part of the network of areas that underlie performance in coarse orientation discrimination. References Adab HZ, Popivanov ID, Vanduffel W, Vogels R (2014) Perceptual Learning of Simple Stimuli Modifies Stimulus Representations in Posterior Inferior Temporal Cortex. J Cogn Neurosci. Keywords: electrical microstimulation, reversible impairment, coarse orientation discrimination, posterior inferior temporal cortex, macaque monkey Conference: Belgian Brain Council 2014 MODULATING THE BRAIN: FACTS, FICTION, FUTURE, Ghent, Belgium, 4 Oct - 4 Oct, 2014. Presentation Type: Poster Presentation Topic: Basic Neuroscience Citation: Zivari Adab H and VOGELS R (2014). Coarse orientation discrimination is impaired by microstimulation of macaque posterior inferior temporal cortex.. Conference Abstract: Belgian Brain Council 2014 MODULATING THE BRAIN: FACTS, FICTION, FUTURE. doi: 10.3389/conf.fnhum.2014.214.00028 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 27 Jun 2014; Published Online: 30 Jun 2014. * Correspondence: Prof. RUFIN VOGELS, KU Leuven, KU Leuven Medical School, Leuven, Please Select, 3000, Belgium, rufin.vogels@kuleuven.be Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Hamed Zivari Adab RUFIN VOGELS Google Hamed Zivari Adab RUFIN VOGELS Google Scholar Hamed Zivari Adab RUFIN VOGELS PubMed Hamed Zivari Adab RUFIN VOGELS Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Large-Scale, High-Resolution Neurophysiological Maps Underlying fMRI of Macaque Temporal Lobe

Maps obtained by functional magnetic resonance imaging (fMRI) are thought to reflect the underlying spatial layout of neural activity. However, previous studies have not been able to directly compare fMRI maps to high-resolution neurophysiological maps, particularly in higher level visual areas. Here, we used a novel stereo microfocal x-ray system to localize thousands of neural recordings across monkey inferior temporal cortex (IT), construct large-scale maps of neuronal object selectivity at subvoxel resolution, and compare those neurophysiology maps with fMRI maps from the same subjects. While neurophysiology maps contained reliable structure at the sub-millimeter scale, fMRI maps of object selectivity contained information at larger scales (>2.5 mm) and were only partly correlated with raw neurophysiology maps collected in the same subjects. However, spatial smoothing of neurophysiology maps more than doubled that correlation, while a variety of alternative transforms led to no significant improvement. Furthermore, raw spiking signals, once spatially smoothed, were as predictive of fMRI maps as local field potential signals. Thus, fMRI of the inferior temporal lobe reflects a spatially low-passed version of neurophysiology signals. These findings strongly validate the widespread use of fMRI for detecting large (>2.5 mm) neuronal domains of object selectivity but show that a complete understanding of even the most pure domains (e.g., faces vs nonface objects) requires investigation at fine scales that can currently only be obtained with invasive neurophysiological methods.

Neural representations of perceptual and semantic identities of individuals in the anterior ventral inferior temporal cortex of monkeys

AbstractSince the discovery of “face cells” in the early 1980s, single‐cell recording experiments in nonhuman primates have made great contributions toward elucidation of the neural mechanisms underlying face perception and recognition. In this article, I review the recent progress in face cell studies, including recent research into the face patches scattered around the anterior temporal cortical areas of monkeys. In particular, I focused on the neural representations of individual identity in these areas. Several groups have shown that the population of face cells in the anterior ventral inferior temporal cortex of monkeys represents the perceptual identity of faces in a view‐invariant manner. In this context, I also summarized our own study showing that the face‐cell population in the anterior ventral inferior temporal cortex of monkeys, which represents the perceptual identity of the faces, can also represent the semantic identity of the individuals; the learned paired associations between an abstract picture and a particular facial identity were also represented in the anterior ventral IT cortex.

Neural plasticity in high-level visual cortex underlying object perceptual learning

With intensive training, human can achieve impressive behavioral improvement on various perceptual tasks. This phenomenon, termed perceptual learning, has long been considered as a hallmark of the plasticity of sensory neural system. Not surprisingly, high-level vision, such as object perception, can also be improved by perceptual learning. Here we review recent psychophysical, electrophysiological, and neuroimaging studies investigating the effects of training on object selective cortex, such as monkey inferior temporal cortex and human lateral occipital area. Evidences show that learning leads to an increase in object selectivity at the single neuron level and/or the neuronal population level. These findings indicate that high-level visual cortex in humans is highly plastic and visual experience can strongly shape neural functions of these areas. At the end of the review, we discuss several important future directions in this area.

Amygdala lesions disrupt modulation of functional MRI activity evoked by facial expression in the monkey inferior temporal cortex

We previously showed that facial expressions modulate functional MRI activity in the face-processing regions of the macaque monkey’s amygdala and inferior temporal (IT) cortex. Specifically, we showed that faces expressing emotion yield greater activation than neutral faces; we term this difference the “valence effect.” We hypothesized that amygdala lesions would disrupt the valence effect by eliminating the modulatory feedback from the amygdala to the IT cortex. We compared the valence effects within the IT cortex in monkeys with excitotoxic amygdala lesions (n = 3) with those in intact control animals (n = 3) using contrast agent-based functional MRI at 3 T. Images of four distinct monkey facial expressions--neutral, aggressive (open mouth threat), fearful (fear grin), and appeasing (lip smack)--were presented to the subjects in a blocked design. Our results showed that in monkeys with amygdala lesions the valence effects were strongly disrupted within the IT cortex, whereas face responsivity (neutral faces > scrambled faces) and face selectivity (neutral faces > non-face objects) were unaffected. Furthermore, sparing of the anterior amygdala led to intact valence effects in the anterior IT cortex (which included the anterior face-selective regions), whereas sparing of the posterior amygdala led to intact valence effects in the posterior IT cortex (which included the posterior face-selective regions). Overall, our data demonstrate that the feedback projections from the amygdala to the IT cortex mediate the valence effect found there. Moreover, these modulatory effects are consistent with an anterior-to-posterior gradient of projections, as suggested by classical tracer studies.