Ivo D. Popivanov

Integration of shape and motion cues in biological motion processing in the monkey STS.

To correctly perceive biological actions, the movement pattern generated in the course of the action has to be linked to the configuration of the actor. Recently, we showed that in humans, motion and configuration cues are processed separately in occipito-temporal cortex, and that both cues are integrated in the extrastriate (EBA) and fusiform (FBA) body areas (Jastorff and Orban, 2009). Using the same factorial design as in our human study, we performed fMRI experiments in awake monkeys to compare biological motion processing in the two species. Point-light displays of monkeys engaged in various actions were presented in a 2×2 factorial design. One factor manipulated the configuration of the stimuli, the other, the kinematics. As in humans, the two factors were anatomically segregated in the superior temporal sulcus (STS) rostral to the MT/V5 complex, with the effect of configuration significant along the lower bank and that of kinematics significant in the fundus and the upper bank of the STS. Moreover, voxels showing a significant interaction between the two factors were mainly confined to body-selective patches within the STS, mimicking our human findings. Importantly, this study reports for the first time differential activation for biological actions presented as point-light displays in the monkey. Moreover, our results suggest that the processing mechanisms of biological actions are remarkably similar in humans and macaque monkeys, and provide the basis for linking existing and future single-cell physiology in the monkey with human functional imaging.

Probabilistic and Single-Subject Retinotopic Maps Reveal the Topographic Organization of Face Patches in the Macaque Cortex

Face perception is crucial to survival among social primates. It has been suggested that a group of extrastriate cortical regions responding more strongly to faces than to nonface objects is critical for face processing in primates. It is generally assumed that these regions are not retinotopically organized, as with human face-processing areas, showing foveal bias but lacking any organization with respect to polar angle. Despite many electrophysiological studies targeting monkey face patches, the retinotopic organization of these patches remains largely unclear. We have examined the relationship between cortical face patches and the topographic organization of extrastriate cortex using biologically relevant, phase-encoded retinotopic mapping stimuli in macaques. Single-subject fMRI results indicated a gradual shift from highly retinotopic to no topographic organization from posterior to anterior face patches in inferotemporal cortex. We also constructed a probabilistic retinotopic atlas of occipital and ventral extrastriate visual cortex. By comparing this probabilistic map to the locations of face patches at the group level, we showed that a previously identified posterior lateral temporal face patch (PL) is located within the posterior inferotemporal dorsal (PITd) retinotopic area. Furthermore, we identified a novel face patch posterior PL, which is located in retinotopically organized transitional area V4 (V4t). Previously published coordinates of human PITd coincide with the group-level occipital face area (OFA), according to a probabilistic map derived from a large population, implying a potential correspondence between monkey PL/PITd and human OFA/PITd. Furthermore, the monkey middle lateral temporal face patch (ML) shows consistent foveal biases but no obvious polar-angle structure. In contrast, middle fundus temporal (MF), anterior temporal and prefrontal monkey face patches lacked topographic organization.

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.

Perceptual learning of simple stimuli modifies stimulus representations in posterior inferior temporal cortex

Practicing simple visual detection and discrimination tasks improves performance, a signature of adult brain plasticity. The neural mechanisms that underlie these changes in performance are still unclear. Previously, we reported that practice in discriminating the orientation of noisy gratings (coarse orientation discrimination) increased the ability of single neurons in the early visual area V4 to discriminate the trained stimuli. Here, we ask whether practice in this task also changes the stimulus tuning properties of later visual cortical areas, despite the use of simple grating stimuli. To identify candidate areas, we used fMRI to map activations to noisy gratings in trained rhesus monkeys, revealing a region in the posterior inferior temporal (PIT) cortex. Subsequent single unit recordings in PIT showed that the degree of orientation selectivity was similar to that of area V4 and that the PIT neurons discriminated the trained orientations better than the untrained orientations. Unlike in previous single unit studies of perceptual learning in early visual cortex, more PIT neurons preferred trained compared with untrained orientations. The effects of training on the responses to the grating stimuli were also present when the animals were performing a difficult orthogonal task in which the grating stimuli were task-irrelevant, suggesting that the training effect does not need attention to be expressed. The PIT neurons could support orientation discrimination at low signal-to-noise levels. These findings suggest that extensive practice in discriminating simple grating stimuli not only affects early visual cortex but also changes the stimulus tuning of a late visual cortical area.

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.