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.

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.

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.

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.

Convolutional neural networks explain tuning properties of anterior, but not middle, face-processing areas in macaque inferotemporal cortex.

Recent computational studies have emphasized layer-wise quantitative similarity between convolutional neural networks (CNNs) and the primate visual ventral stream. However, whether such similarity holds for the face-selective areas, a subsystem of the higher visual cortex, is not clear. Here, we extensively investigate whether CNNs exhibit tuning properties as previously observed in different macaque face areas. While simulating four past experiments on a variety of CNN models, we sought for the model layer that quantitatively matches the multiple tuning properties of each face area. Our results show that higher model layers explain reasonably well the properties of anterior areas, while no layer simultaneously explains the properties of middle areas, consistently across the model variation. Thus, some similarity may exist between CNNs and the primate face-processing system in the near-goal representation, but much less clearly in the intermediate stages, thus requiring alternative modeling such as non-layer-wise correspondence or different computational principles.

Significance of Natural Scene Statistics in Understanding the Anisotropies of Perceptual Filling-in at the Blind Spot.

Psychophysical experiments reveal our horizontal preference in perceptual filling-in at the blind spot. On the other hand, tolerance in filling-in exhibit vertical preference. What causes this anisotropy in our perception? Building upon the general notion that the functional properties of the early visual system are shaped by the innate specification as well as the statistics of the environment, we reasoned that the anisotropy in filling-in could be understood in terms of anisotropy in orientation distribution inherent in natural scene statistics. We examined this proposition by investigating filling-in of bar stimuli in a Hierarchical Predictive Coding model network. The model network, trained with natural images, exhibited anisotropic filling-in performance at the blind spot, which is similar to the findings of psychophysical experiments. We suggest that the over-representation of horizontal contours in the natural scene contributes to the observed horizontal superiority in filling-in and the broader distribution of vertical contours contributes to the observed vertical superiority of tolerance in filling-in. These results indicate that natural scene statistics plays a significant role in determining the filling-in performance at the blind spot and shaping the associated anisotropies.

Predictive Coding: A Possible Explanation of Filling-In at the Blind Spot.

Filling-in at the blind spot is a perceptual phenomenon in which the visual system fills the informational void, which arises due to the absence of retinal input corresponding to the optic disc, with surrounding visual attributes. It is known that during filling-in, nonlinear neural responses are observed in the early visual area that correlates with the perception, but the knowledge of underlying neural mechanism for filling-in at the blind spot is far from complete. In this work, we attempted to present a fresh perspective on the computational mechanism of filling-in process in the framework of hierarchical predictive coding, which provides a functional explanation for a range of neural responses in the cortex. We simulated a three-level hierarchical network and observe its response while stimulating the network with different bar stimulus across the blind spot. We find that the predictive-estimator neurons that represent blind spot in primary visual cortex exhibit elevated non-linear response when the bar stimulated both sides of the blind spot. Using generative model, we also show that these responses represent the filling-in completion. All these results are consistent with the finding of psychophysical and physiological studies. In this study, we also demonstrate that the tolerance in filling-in qualitatively matches with the experimental findings related to non-aligned bars. We discuss this phenomenon in the predictive coding paradigm and show that all our results could be explained by taking into account the efficient coding of natural images along with feedback and feed-forward connections that allow priors and predictions to co-evolve to arrive at the best prediction. These results suggest that the filling-in process could be a manifestation of the general computational principle of hierarchical predictive coding of natural images.