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.

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.

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.

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.

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.

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.

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.

Transformation of Visual Representations Across Ventral Stream Body-selective Patches.

Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex.

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.

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.

A behavioral face preference deficit in a monkey with an incomplete face patch system.

Primates are experts in face perception and naturally show a preference for faces under free-viewing conditions. The primate ventral stream is characterized by a network of face patches that selectively responds to faces, but it remains uncertain how important such parcellation is for face perception. Here we investigated free-viewing behavior in a female monkey who naturally lacks fMRI-defined posterior and middle lateral face patches. We presented a series of content-rich images of scenes that included faces or other objects to that monkey during a free-viewing task and tested a group of 10 control monkeys on the same task for comparison. We found that, compared to controls, the monkey with missing face patches showed a marked reduction of face viewing preference that was most pronounced for the first few fixations. In addition, her gaze fixation patterns were substantially distinct from those of controls, especially for pictures with a face. These data demonstrate an association between the clustering of neurons in face selective patches and a behavioral bias for faces in natural images.

Representations of regular and irregular shapes by deep Convolutional Neural Networks, monkey inferotemporal neurons and human judgments.

Recent studies suggest that deep Convolutional Neural Network (CNN) models show higher representational similarity, compared to any other existing object recognition models, with macaque inferior temporal (IT) cortical responses, human ventral stream fMRI activations and human object recognition. These studies employed natural images of objects. A long research tradition employed abstract shapes to probe the selectivity of IT neurons. If CNN models provide a realistic model of IT responses, then they should capture the IT selectivity for such shapes. Here, we compare the activations of CNN units to a stimulus set of 2D regular and irregular shapes with the response selectivity of macaque IT neurons and with human similarity judgements. The shape set consisted of regular shapes that differed in nonaccidental properties, and irregular, asymmetrical shapes with curved or straight boundaries. We found that deep CNNs (Alexnet, VGG-16 and VGG-19) that were trained to classify natural images show response modulations to these shapes that were similar to those of IT neurons. Untrained CNNs with the same architecture than trained CNNs, but with random weights, demonstrated a poorer similarity than CNNs trained in classification. The difference between the trained and untrained CNNs emerged at the deep convolutional layers, where the similarity between the shape-related response modulations of IT neurons and the trained CNNs was high. Unlike IT neurons, human similarity judgements of the same shapes correlated best with the last layers of the trained CNNs. In particular, these deepest layers showed an enhanced sensitivity for straight versus curved irregular shapes, similar to that shown in human shape judgments. In conclusion, the representations of abstract shape similarity are highly comparable between macaque IT neurons and deep convolutional layers of CNNs that were trained to classify natural images, while human shape similarity judgments correlate better with the deepest layers.

Statistical Learning Signals in Macaque Inferior Temporal Cortex.

Humans are sensitive to statistical regularities in their visual environment, but the nature of the underlying neural statistical learning signals still remains to be clarified. As in human behavioral and neuroimaging studies of statistical learning, we exposed rhesus monkeys to a continuous stream of images, presented without interstimulus interval or reward association. The stimulus set consisted of 3 groups of 5 images each (quintets). The stimulus order within each quintet was fixed, but the quintets were presented repeatedly in a random order without interruption. Thus, only transitional probabilities defined quintets of images. Postexposure recordings in inferior temporal (IT) cortex showed an enhanced response to stimuli that violated the exposed sequence. This enhancement was found only for stimuli that were not predicted by the just preceding stimulus, reflecting a temporally adjacent stimulus relationship, and was sensitive to stimulus order. By comparing IT responses with sequences with and without statistical regularities, we observed a short latency, transient response suppression for stimuli of the sequence with regularities, in addition to a later sustained response enhancement to stimuli that violated the sequence with regularities. These findings constrain models of mechanisms underlying neural responses in predictable temporal sequences, such as predictive coding.

Stimulus features coded by single neurons of a macaque body category selective patch.

Body category-selective regions of the primate temporal cortex respond to images of bodies, but it is unclear which fragments of such images drive single neurons' responses in these regions. Here we applied the Bubbles technique to the responses of single macaque middle superior temporal sulcus (midSTS) body patch neurons to reveal the image fragments the neurons respond to. We found that local image fragments such as extremities (limbs), curved boundaries, and parts of the torso drove the large majority of neurons. Bubbles revealed the whole body in only a few neurons. Neurons coded the features in a manner that was tolerant to translation and scale changes. Most image fragments were excitatory but for a few neurons both inhibitory and excitatory fragments (opponent coding) were present in the same image. The fragments we reveal here in the body patch with Bubbles differ from those suggested in previous studies of face-selective neurons in face patches. Together, our data indicate that the majority of body patch neurons respond to local image fragments that occur frequently, but not exclusively, in bodies, with a coding that is tolerant to translation and scale. Overall, the data suggest that the body category selectivity of the midSTS body patch depends more on the feature statistics of bodies (e.g., extensions occur more frequently in bodies) than on semantics (bodies as an abstract category).

Divisive Normalization Predicts Adaptation-Induced Response Changes in Macaque Inferior Temporal Cortex.

UNLABELLED: Stimulus repetition alters neural responses to the repeated stimulus. This so-called adaptation phenomenon has been commonly observed at multiple spatial and temporal scales and in different brain areas, and has been hypothesized to affect the neural representation of the sensory input. Yet, the neural mechanisms underlying adaptation still remain unclear, especially in higher-order cortical areas. Here we employ a divisive normalization model of neural responses to predict adaptation-induced changes in responses of single neurons in the macaque inferior temporal (IT) cortex. According to this model, the response of a neuron is determined by an interplay between its direct excitatory and divisive normalizing inputs, with each input being subject to adaptation. To test the model, we recorded the responses of single IT cortex neurons to complex visual stimuli while separately adapting the two putative types of input to those neurons. We compared the changes in responses of these neurons following such adaptation with predictions derived from the divisive normalization model. As predicted by the model, we show that adaptation in the IT cortex can, depending on the relative strength of each putative type of input to a neuron, suppress or enhance the neural response to a complex stimulus. More generally, our data suggest that adaptation serves to selectively enhance processing of the stimuli that differ from recently experienced ones, even when these occur within a configuration of multiple stimuli. SIGNIFICANCE STATEMENT: Stimulus repetition alters neural responses to the repeated stimulus. This so-called adaptation phenomenon has been robustly demonstrated in brains of different species and is considered to be a form of short-term plasticity inherent to the processing of sensory stimuli. Nevertheless, the functional role and underlying mechanisms of adaptation remain unclear. Here we demonstrate that divisive normalization, a canonical neural computation operating throughout the brain, predicts the adaptation-induced changes in response of single neurons to complex stimulus configurations in the macaque inferotemporal cortex. Our findings embed adaptation effects of inferotemporal neurons into the context of a broader neural network perspective that includes divisive normalization. Additionally, our findings have implications for understanding of the function of adaptation in higher-order sensory cortices.

Encoding of Predictable and Unpredictable Stimuli by Inferior Temporal Cortical Neurons.

Animals and humans learn statistical regularities that are embedded in sequences of stimuli. The neural mechanisms of such statistical learning are still poorly understood. Previous work in macaque inferior temporal (IT) cortex demonstrated suppressed spiking activity to visual images of a sequence in which the stimulus order was defined by transitional probabilities (labeled as "standard" sequence), compared with a sequence in which the stimulus order was random ("random" sequence). Here, we asked whether IT neurons encode the images of the standard sequence more accurately compared with images of the random sequence. Previous human fMRI studies in different sensory modalities also found a suppressed response to expected relative to unexpected stimuli but obtained various results regarding the effect of expectation on encoding, with one study reporting an improved classification accuracy of expected stimuli despite the reduced activation level. We employed a linear classifier to decode image identity from the spiking responses of the recorded IT neurons. We found a greater decoding accuracy for images of the standard compared with the random sequence during the early part of the stimulus presentation, but further analyses suggested that this reflected the sustained, stimulus-selective activity from the previous stimulus of the sequence, which is typical for IT neurons. However, the peak decoding accuracy was lower for the standard compared with the random sequence, in line with the reduced response to the former compared with the latter images. These data suggest that macaque IT neurons represent less accurately predictable compared with unpredictable images.

Perturbation of Posterior Inferior Temporal Cortical Activity Impairs Coarse Orientation Discrimination.

It is reasonable to assume that the discrimination of simple visual stimuli depends on the activity of early visual cortical neurons, because simple visual features are supposedly coded in these areas whereas more complex features are coded in late visual areas. Recently, we showed that training monkeys in a coarse orientation discrimination task modified the response properties of single neurons in the posterior inferior temporal (PIT) cortex, a late visual area. Here, we examined the contribution of PIT to coarse orientation discrimination using causal perturbation methods. Electrical stimulation (ES) of PIT with currents of at least 100 µA impaired coarse orientation discrimination in monkeys. The performance deterioration did not exclusively reflect a general impairment to perform a difficult perceptual task. However, high current (650 µA) but not low-current (100 µA) ES also impaired fine color discrimination. ES of temporal regions dorsal or anterior to PIT produced less impairment of coarse orientation discrimination than ES of PIT. Injections of the GABA agonist muscimol into PIT also impaired performance. These data suggest that the late cortical area PIT is part of the network that supports coarse orientation discrimination of a simple grating stimulus, at least after extensive training in this task at threshold.

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.

Repetition suppression for visual actions in the macaque superior temporal sulcus.

In many brain areas, repetition of a stimulus usually weakens the neural response. This "adaptation" or repetition suppression effect has been observed with mass potential measures such as event-related potentials (ERPs), in fMRI BOLD responses, and locally with local field potentials (LFPs) and spiking activity. Recently, it has been reported that macaque F5 mirror neurons do not show repetition suppression of their spiking activity for single repetitions of hand actions, which disagrees with human fMRI adaptation studies. This finding also contrasts with numerous studies showing repetition suppression in macaque inferior temporal cortex, including the rostral superior temporal sulcus (STS). Since the latter studies employed static stimuli, we assessed here whether the use of dynamic action stimuli abolishes repetition suppression in the awake macaque STS. To assess adaptation effects in the STS, we employed the same hand action movies as used when examining adaptation in F5. The upper bank STS neurons showed repetition suppression during the approaching phase of the hand action, which corresponded to the phase of the action for which these neurons responded overall the strongest. The repetition suppression was present for the spiking activity measured in independent single-unit and multiunit recordings as well as for the LFP power at frequencies > 50 Hz. Together with previous data in F5, these findings suggest that adaptation effects differ between F5 mirror neurons and the STS neurons.

Neurons in macaque inferior temporal cortex show no surprise response to deviants in visual oddball sequences.

Many studies measured neural responses in oddball paradigms, showing a different response to the same stimulus when presented with a low (deviant) compared with a high probability (standard) in a sequence. Such a differential response is manifested in event-related potential studies as the mismatch negativity (MMN) and has been observed in several sensory modalities, including vision. Other studies showed that stimulus repetition suppresses the neural response. It has been suggested that this adaptation effect underlies the smaller responses to the standard compared with the deviant stimulus in oddball sequences. However, the MMN may also reflect the violation of a prediction based on the sequence of standards, i.e., a surprise response. We examined the presence of a surprise response to deviants in visual oddball sequences in macaque (Macaca mulatta) inferior temporal (IT) cortex, a higher-order cortical area. In agreement with visual MMN studies, single-unit IT responses were greater for the deviant than for the standard stimuli. However, single IT neurons showed no greater response to the deviant stimulus in the oddball sequence than to the same stimulus presented with the same probability in a sequence that consisted of many stimuli. LFPs also showed no evidence of a surprise response. These data suggest that stimulus-specific adaptation, without a surprise-related boost of activity to the deviant, underlies the responses in visual oddball sequences even in higher visual cortex. Furthermore, we show that for IT neurons such adaptive mechanisms take into account a relatively short stimulus history, with weaker effects at longer time scales.