Location-specific deviant responses to object sequences in macaque inferior temporal cortex.

Many species learn temporal regularities in their visual environment, demonstrating visual statistical learning. In this study, we explored the sensitivity of macaque inferior temporal (IT) cortical neurons to transition probabilities of sequentially presented visual images, presented at different locations in the visual field. We exposed monkeys to sequences of two images, where the first image was presented either foveally or peripherally, and the second image was consistently presented foveally. Following several weeks of exposure, we recorded IT responses to assess differences between the exposed (Fixed) and new, Deviant sequences, where the identity of the first image in a sequence differed from the exposure phase. While enhanced responses to Deviant sequences were observed when both images of a pair were foveally presented during exposure, no such deviant responses were present when the first image was presented peripherally. This finding challenges the notion that mere exposure to image sequences always leads to deviant responses in macaque IT. The results highlight the complexity of the mechanisms underlying statistical learning in primates, particularly in the context of peripheral image presentations, emphasizing the need for further investigation into the origins of these responses in the IT cortex.

Configuration-sensitive face-body interactions in primate visual cortex.

Traditionally, the neural processing of faces and bodies is studied separately, although they are encountered together, as parts of an agent. Despite its social importance, it is poorly understood how faces and bodies interact, particularly at the single-neuron level. Here, we examined the interaction between faces and bodies in the macaque inferior temporal (IT) cortex, targeting an fMRI-defined patch. We recorded responses of neurons to monkey images in which the face was in its natural location (natural face-body configuration), or in which the face was mislocated with respect to the upper body (unnatural face-body configuration). On average, the neurons did not respond stronger to the natural face-body configurations compared to the summed responses to their faces and bodies, presented in isolation. However, the neurons responded stronger to the natural compared to the unnatural face-body configurations. This configuration effect was present for face- and monkey-centered images, did not depend on local feature differences between configurations, and was present when the face was replaced by a small object. The face-body interaction rules differed between natural and unnatural configurations. In sum, we show for the first time that single IT neurons process faces and bodies in a configuration-specific manner, preferring natural face-body configurations.

Bodies in motion: Unraveling the distinct roles of motion and shape in dynamic body responses in the temporal cortex.

The temporal cortex represents social stimuli, including bodies. We examine and compare the contributions of dynamic and static features to the single-unit responses to moving monkey bodies in and between a patch in the anterior dorsal bank of the superior temporal sulcus (dorsal patch [DP]) and patches in the anterior inferotemporal cortex (ventral patch [VP]), using fMRI guidance in macaques. The response to dynamics varies within both regions, being higher in DP. The dynamic body selectivity of VP neurons correlates with static features derived from convolutional neural networks and motion. DP neurons' dynamic body selectivity is not predicted by static features but is dominated by motion. Whereas these data support the dominance of motion in the newly proposed "dynamic social perception" stream, they challenge the traditional view that distinguishes DP and VP processing in terms of motion versus static features, underscoring the role of inferotemporal neurons in representing body dynamics.

Stimulus expectations do not modulate visual event-related potentials in probabilistic cueing designs.

Humans and other animals can learn and exploit repeating patterns that occur within their environments. These learned patterns can be used to form expectations about future sensory events. Several influential predictive coding models have been proposed to explain how learned expectations influence the activity of stimulus-selective neurons in the visual system. These models specify reductions in neural response measures when expectations are fulfilled (termed expectation suppression) and increases following surprising sensory events. However, there is currently scant evidence for expectation suppression in the visual system when confounding factors are taken into account. Effects of surprise have been observed in blood oxygen level dependent (BOLD) signals, but not when using electrophysiological measures. To provide a strong test for expectation suppression and surprise effects we performed a predictive cueing experiment while recording electroencephalographic (EEG) data. Participants (n=48) learned cue-face associations during a training session and were then exposed to these cue-face pairs in a subsequent experiment. Using univariate analyses of face-evoked event-related potentials (ERPs) we did not observe any differences across expected (90% probability), neutral (50%) and surprising (10%) face conditions. Across these comparisons, Bayes factors consistently favoured the null hypothesis throughout the time-course of the stimulus-evoked response. When using multivariate pattern analysis we did not observe above-chance classification of expected and surprising face-evoked ERPs. By contrast, we found robust within- and across-trial stimulus repetition effects. Our findings do not support predictive coding-based accounts that specify reduced prediction error signalling when perceptual expectations are fulfilled. They instead highlight the utility of other types of predictive processing models that describe expectation-related phenomena in the visual system without recourse to prediction error signalling.

Perceptual learning: Breaking specificity by variability.

A new psychophysical study in humans suggests that increasing the variability of task-irrelevant features during training enhances the generalization of visual perceptual learning to untrained stimuli and locations.

Inferior temporal cortex leads prefrontal cortex in response to a violation of a learned sequence.

Primates learn statistical regularities that are embedded in visual sequences, a form of statistical learning. Single-unit recordings in macaques showed that inferior temporal (IT) neurons are sensitive to statistical regularities in visual sequences. Here, we asked whether ventrolateral prefrontal cortex (VLPFC), which is connected to IT, is also sensitive to the transition probabilities in visual sequences and whether the statistical learning signal in IT originates in VLPFC. We recorded simultaneously multiunit activity (MUA) and local field potentials (LFPs) in IT and VLPFC after monkeys were exposed to triplets of images with a fixed presentation order. In both areas, the MUA was stronger to images that violated the learned sequence (deviants) compared to the same images presented in the learned triplets. The high-gamma and beta LFP power showed an enhanced and suppressed response, respectively, to the deviants in both areas. The enhanced response was present also for the image following the deviant, suggesting a sensitivity for temporal adjacent dependencies in IT and VLPFC. The increased response to the deviant occurred later in VLPFC than in IT, suggesting that the deviant response in IT was not inherited from VLPFC. These data support predictive coding theories that propose a feedforward flow of prediction errors.

Categorization learning induced changes in action representations in the macaque STS.

Neuroimaging and single cell recordings have demonstrated the presence of STS body category-selective regions (body patches) containing neurons responding to presentation of static bodies and body parts. To date, it remains unclear if these body patches and additional STS regions respond during observation of different categories of dynamic actions and to what extent categorization learning influences representations of observed actions in the STS. In the present study, we trained monkeys to discriminate videos depicting three different actions categories (grasping, touching and reaching) with a forced-choice action categorization task. Before and after categorization training, we performed fMRI recordings while monkeys passively observed the same action videos. At the behavioral level, after categorization training, monkeys generalized to untrained action exemplars, in particular for grasping actions. Before training, uni- and/or multivariate fMRI analyses suggest a broad representation of dynamic action categories in particular in posterior and middle STS. Univariate analysis further suggested action category specific training effects in middle and anterior body patches, face patch ML and posterior STS region MT and FST. Overall, our fMRI experiments suggest a widespread representation of observed dynamic bodily actions in the STS that can be modulated by visual learning, supporting its proposed role in action recognition.

A large-scale brain network of species-specific dynamic human body perception.

This ultrahigh field 7 T fMRI study addressed the question of whether there exists a core network of brain areas at the service of different aspects of body perception. Participants viewed naturalistic videos of monkey and human faces, bodies, and objects along with mosaic-scrambled videos for control of low-level features. Independent component analysis (ICA) based network analysis was conducted to find body and species modulations at both the voxel and the network levels. Among the body areas, the highest species selectivity was found in the middle frontal gyrus and amygdala. Two large-scale networks were highly selective to bodies, dominated by the lateral occipital cortex and right superior temporal sulcus (STS) respectively. The right STS network showed high species selectivity, and its significant human body-induced node connectivity was focused around the extrastriate body area (EBA), STS, temporoparietal junction (TPJ), premotor cortex, and inferior frontal gyrus (IFG). The human body-specific network discovered here may serve as a brain-wide internal model of the human body serving as an entry point for a variety of processes relying on body descriptions as part of their more specific categorization, action, or expression recognition functions.

Keep the head in the right place: Face-body interactions in inferior temporal cortex.

In primates, faces and bodies activate distinct regions in the inferior temporal (IT) cortex and are typically studied separately. Yet, primates interact with whole agents and not with random concatenations of faces and bodies. Despite its social importance, it is still poorly understood how faces and bodies interact in IT. Here, we addressed this gap by measuring fMRI activations to whole agents and to unnatural face-body configurations in which the head was mislocated with respect to the body, and examined how these relate to the sum of the activations to their corresponding faces and bodies. First, we mapped patches in the IT of awake macaques that were activated more by images of whole monkeys compared to objects and found that these mostly overlapped with body and face patches. In a second fMRI experiment, we obtained no evidence for superadditive responses in these "monkey patches", with the activation to the monkeys being less or equal to the summed face-body activations. However, monkey patches in the anterior IT were activated more by natural compared to unnatural configurations. The stronger activations to natural configurations could not be explained by the summed face-body activations. These univariate results were supported by regression analyses in which we modeled the activations to both configurations as a weighted linear combination of the activations to the faces and bodies, showing higher regression coefficients for the natural compared to the unnatural configurations. Deeper layers of trained convolutional neural networks also contained units that responded more to natural compared to unnatural monkey configurations. Unlike the monkey fMRI patches, these units showed substantial superadditive responses to the natural configurations. Our monkey fMRI data suggest configuration-sensitive face-body interactions in anterior IT, adding to the evidence for an integrated face-body processing in the primate ventral visual stream, and open the way for mechanistic studies using single unit recordings in these patches.

More Than the Face: Representations of Bodies in the Inferior Temporal Cortex.

Visual representations of bodies, in addition to those of faces, contribute to the recognition of con- and heterospecifics, to action recognition, and to nonverbal communication. Despite its importance, the neural basis of the visual analysis of bodies has been less studied than that of faces. In this article, I review what is known about the neural processing of bodies, focusing on the macaque temporal visual cortex. Early single-unit recording work suggested that the temporal visual cortex contains representations of body parts and bodies, with the dorsal bank of the superior temporal sulcus representing bodily actions. Subsequent functional magnetic resonance imaging studies in both humans and monkeys showed several temporal cortical regions that are strongly activated by bodies. Single-unit recordings in the macaque body patches suggest that these represent mainly body shape features. More anterior patches show a greater viewpoint-tolerant selectivity for body features, which may reflect a processing principle shared with other object categories, including faces.

Limited Pairings of Electrical Micro-stimulation of the Ventral Tegmental Area and a Visual Stimulus Enhance Visual Cortical Responses.

Previous studies demonstrated that pairing a visual stimulus and electrical micro-stimulation of the ventral tegmental area (VTA-EM) for multiple days is sufficient to induce visual cortical plasticity and changes perception. However, a brief epoch of VTA-EM-stimulus pairing within a single day has been shown to result in a behavioral preference for the paired stimulus. Here, we investigated whether a brief single-day session of VTA-EM-stimulus pairings is sufficient to induce changes in visual cortical responses. We examined macaque posterior inferior temporal (PIT) cortex because previous studies demonstrated response changes after VTA-EM stimulus pairing in that area. Multi-unit recordings in PIT were interleaved with VTA-EM-stimulus pairing epochs. During the short VTA-EM-stimulus pairing epochs (60 pairings), one image (fractal) was paired with VTA-EM (STIM) whereas another, unpaired fractal was presented as control. Two other fractals (dummies) were presented only during the recordings. The difference in response between the STIM and control fractals already increased after the first VTA-EM-stimulus pairing epoch, reflecting a relative increase of the response to the STIM fractal. However, the response to the STIM fractal did not increase further with more VTA-EM-stimulus pairing epochs. The relative increase in firing rate for the paired fractal was present early in the response, in line with a local/ bottom-up origin. These effects were absent when comparing the responses to the dummies pre- and post-VTA-EM. This study shows that pairing a visual image and VTA-EM in a brief single-day session is sufficient to increase the response for the paired image in macaque PIT.

It is not just the category: behavioral effects of fMRI-guided electrical microstimulation result from a complex interplay of factors.

Functional imaging and electrophysiological studies in primates revealed the existence of patches selective for visual categories in the inferior temporal cortex. Understanding the contribution of these patches to perception requires causal techniques that assess the effect of neural activity manipulations on perception. We used electrical microstimulation (EM) to determine the role of body patch activity in visual categorization in macaques. We tested the hypothesis that EM in a body patch would affect the categorization of bodies versus objects but not of other visual categories. We employed low-current EM of an anterior body patch (ASB) in the superior temporal sulcus, which was defined by functional magnetic resonance imaging and verified with electrophysiological recordings in each session. EM of ASB affected body categorization, but the EM effects were more complex than the expected increase of body-related choices: EM affected the categorization of both body and inanimate images and showed interaction with the choice target location, but its effect was location-specific (tested in 1 subject) on a millimeter scale. Our findings suggest that the behavioral effects of EM in a category-selective patch are not merely a manifestation of the category selectivity of the underlying neuronal population but reflect a complex interplay of multiple factors.

Stimulation of the ventral tegmental area induces visual cortical plasticity at the neuronal level.

fMRI studies have shown that pairing a task-irrelevant visual feature with electrical micro-stimulation of the ventral tegmental area (VTA-EM) is sufficient to increase the sensory cortical representation of the paired feature and to improve perceptual performance. However, since fMRI provides an indirect measure of neural activity, the neural response changes underlying the fMRI activations are unknown. Here, we pair a task-irrelevant grating orientation with VTA-EM while attention is directed to a difficult orthogonal task. We examine the changes in neural response properties in macaques by recording spiking activity in the posterior inferior temporal cortex, the locus of fMRI-defined plasticity in previous studies. We observe a relative increase in mean spike rate and preference for the VTA-EM paired orientation compared to an unpaired orientation, which is unrelated to attention. These results demonstrate that VTA-EM-stimulus pairing is sufficient to induce sensory cortical plasticity at the spiking level in nonhuman primates.

Moving a Shape behind a Slit: Partial Shape Representations in Inferior Temporal Cortex.

Current models of object recognition are based on spatial representations build from object features that are simultaneously present in the retinal image. However, one can recognize an object when it moves behind a static occlude, and only a small fragment of its shape is visible through a slit at a given moment in time. Such anorthoscopic perception requires spatiotemporal integration of the successively presented shape parts during slit-viewing. Human fMRI studies suggested that ventral visual stream areas represent whole shapes formed through temporal integration during anorthoscopic perception. To examine the time course of shape-selective responses during slit-viewing, we recorded the responses of single inferior temporal (IT) neurons of rhesus monkeys to moving shapes that were only partially visible through a static narrow slit. The IT neurons signaled shape identity by their response when that was cumulated across the duration of the shape presentation. Their shape preference during slit-viewing equaled that for static, whole-shape presentations. However, when analyzing their responses at a finer time scale, we showed that the IT neurons responded to particular shape fragments that were revealed by the slit. We found no evidence for temporal integration of slit-views that result in a whole-shape representation, even when the monkey was matching slit-views of a shape to static whole-shape presentations. These data suggest that, although the temporally integrated response of macaque IT neurons can signal shape identity in slit-viewing conditions, the spatiotemporal integration needed for the formation of a whole-shape percept occurs in other areas, perhaps downstream to IT.SIGNIFICANCE STATEMENT One recognizes an object when it moves behind a static occluder and only a small fragment of its shape is visible through a static slit at a given moment in time. Such anorthoscopic perception requires spatiotemporal integration of the successively presented partial shape parts. Human fMRI studies suggested that ventral visual stream areas represent shapes formed through temporal integration. We recorded the responses of inferior temporal (IT) cortical neurons of macaques during slit-viewing conditions. Although the temporally summated response of macaque IT neurons could signal shape identity under slit-viewing conditions, we found no evidence for a whole-shape representation using analyses at a finer time scale. Thus, the spatiotemporal integration needed for anorthoscopic perception does not occur within IT.

Long term fMRI adaptation depends on adapter response in face-selective cortex.

Repetition suppression (RS) reflects a neural attenuation during repeated stimulation. We used fMRI and the subsequent memory paradigm to test the predictive coding hypothesis for RS during visual memory processing by investigating the interaction between RS and differences due to memory in category-selective cortex (FFA, pSTS, PPA, and RSC). Fifty-six participants encoded face and house stimuli twice, followed by an immediate and delayed (48 h) recognition memory assessment. Linear Mixed Model analyses with repetition, subsequent recognition performance, and their interaction as fixed effects revealed that absolute RS during encoding interacts with probability of future remembrance in face-selective cortex. This effect was not observed for relative RS, i.e. when controlled for adapter-response. The findings also reveal an association between adapter response and RS, both for short and long term (48h) intervals, after controlling for the mathematical dependence between both measures. These combined findings are challenging for predictive coding models of visual memory and are more compatible with adapter-related and familiarity accounts.

Evaluating the evidence for expectation suppression in the visual system.

Reports of expectation suppression have shaped the development of influential predictive coding-based theories of visual perception. However recent work has highlighted confounding factors that may mimic or inflate expectation suppression effects. In this review, we describe four confounds that are prevalent across experiments that tested for expectation suppression: effects of surprise, attention, stimulus repetition and adaptation, and stimulus novelty. With these confounds in mind we then critically review the evidence for expectation suppression across probabilistic cueing, statistical learning, oddball, action-outcome learning and apparent motion designs. We found evidence for expectation suppression within a specific subset of statistical learning designs that involved weeks of sequence learning prior to neural activity measurement. Across other experimental contexts, whereby stimulus appearance probabilities were learned within one or two testing sessions, there was inconsistent evidence for genuine expectation suppression. We discuss how an absence of expectation suppression could inform models of predictive processing, repetition suppression and perceptual decision-making. We also provide suggestions for designing experiments that may better test for expectation suppression in future work.

Electrical stimulation of the macaque ventral tegmental area drives category-selective learning without attention.

Perception improves by repeated practice with visual stimuli, a phenomenon known as visual perceptual learning (VPL). The interplay of attentional and neuromodulatory reward signals is hypothesized to cause these behavioral and associated neuronal changes, although VPL can occur without attention (i.e., task-irrelevant VPL). In addition, task-relevant VPL can be category-selective for simple attended oriented stimuli. Yet, it is unclear whether category-selective task-irrelevant VPL occurs and which brain centers mediate underlying forms of adult cortical plasticity. Here, we show that pairing subliminal complex visual stimuli (faces and bodies) with electrical microstimulation of the ventral tegmental area (VTA-EM) causes category-selective task-irrelevant VPL. These perceptual improvements are accompanied by fMRI signal changes in early and late visual and frontal areas, as well as the cerebellum, hippocampus, claustrum, and putamen. In conclusion, Pavlovian pairing of unattended complex stimuli with VTA-EM causes category-selective learning accompanied by changes of cortical and subcortical neural representations in macaques.

Within- and between-hemifield generalization of repetition suppression in inferior temporal cortex.

The decrease in response with stimulus repetition is a common property observed in many sensory brain areas. This repetition suppression (RS) is ubiquitous in neurons of macaque inferior temporal (IT) cortex, the end-stage of the ventral visual pathway. The neural mechanisms of RS in IT are still unclear, and one possibility is that it is inherited from areas upstream to IT that show also RS. Since neurons in IT have larger receptive fields compared with earlier visual areas, we examined the inheritance hypothesis by presenting adapter and test stimuli at widely different spatial locations along both vertical and horizontal meridians and across hemifields. RS was present for distances between adapter and test stimuli up to 22° and when the two stimuli were presented in different hemifields. Also, we examined the position tolerance of the stimulus selectivity of adaptation by comparing the responses to a test stimulus following the same (repetition trial) or a different (alternation trial) adapter at a position different from the test stimulus. Stimulus-selective adaptation was still present and consistently stronger in the later phase of the response for distances up to 18°. Finally, we observed stimulus-selective adaptation in repetition trials even without a measurable excitatory response to the adapter stimulus. To accommodate these and previous data, we propose that at least part of the stimulus-selective adaptation in IT is based on short-term plasticity mechanisms within IT and/or reflects top-down activity from areas downstream to IT.NEW & NOTEWORTHY Neurons in inferior temporal cortex reduce their response when stimuli are repeated. To assess whether this repetition suppression is inherited from upstream visual areas, we examined the extent of its spatial generalization. We observed stimulus-selective adaptation when adapter and test stimuli were presented at widely different spatial positions and in different hemifields. These data suggest that at least part of the repetition suppression originates within inferior temporal cortex and/or reflects feedback from downstream areas.

Statistical Learning Signals for Complex Visual Images in Macaque Early Visual Cortex.

Animals of several species, including primates, learn the statistical regularities of their environment. In particular, they learn the temporal regularities that occur in streams of visual images. Previous human neuroimaging studies reported discrepant effects of such statistical learning, ranging from stronger occipito-temporal activations for sequences in which image order was fixed, compared with sequences of randomly ordered images, to weaker activations for fixed-order sequences compared with sequences that violated the learned order. Several single-unit studies in macaque monkeys reported that after statistical learning of temporal regularities, inferior temporal (IT) neurons show reduced responses to learned fixed-order sequences of visual images compared with random or mispredicted sequences. However, it is unknown how other macaque brain areas respond to such temporal statistical regularities. To address this gap, we exposed rhesus monkeys (Macaca mulatta) to two types of sequences of complex images. The "regular" sequences consisted of a continuous stream of quartets, and within each quartet, the image order was fixed. The quartets themselves were displayed, uninterrupted, in a random order. The same monkeys were exposed to sequences of other images having a pseudorandomized order ("random" sequence). After exposure, both monkeys were scanned with functional MRI (fMRI) using a block design with three conditions: regular sequence, random sequence, and fixation-only blocks. A whole-brain analysis showed a reduced activation in mainly the occipito-temporal cortex for the regular compared to the random sequences. Marked response reductions for the regular sequence were observed in early extrastriate visual cortical areas, including area V2, despite the use of rather complex images of animals. These data suggest that statistical learning signals are already present in early visual areas of monkeys, even for complex visual images. These monkey fMRI data are in line with recent human fMRI studies that showed a reduced activation in early visual areas for predicted compared with mispredicted complex images.

Body Patches in Inferior Temporal Cortex Encode Categories with Different Temporal Dynamics.

An unresolved question in cognitive neuroscience is how representations of object categories at different levels (basic and superordinate) develop during the course of the neural response within an area. To address this, we decoded categories of different levels from the spiking responses of populations of neurons recorded in two fMRI-defined body patches in the macaque STS. Recordings of the two patches were made in the same animals with the same stimuli. Support vector machine classifiers were trained at brief response epochs and tested at the same or different epochs, thus assessing whether category representations change during the course of the response. In agreement with hierarchical processing within the body patch network, the posterior body patch mid STS body (MSB) showed an earlier onset of categorization compared with the anterior body patch anterior STS body (ASB), irrespective of the categorization level. Decoding of the superordinate body versus nonbody categories was less dynamic in MSB than in ASB, with ASB showing a biphasic temporal pattern. Decoding of the ordinate-level category human versus monkey bodies showed similar temporal patterns in both patches. The decoding onset of superordinate categorizations involving bodies was as early as for basic-level categorization, suggesting that previously reported differences between the onset of basic and superordinate categorizations may depend on the area. The qualitative difference between areas in their dynamics of category representation may hinder the interpretation of decoding dynamics based on EEG or MEG, methods that may mix signals of different areas.