Three studies investigate neural activity in the ventral pathway, including the inferotemporal cortex (IT), each using a novel experimental approach. The overall focus is on how the brain processes dynamic, social stimuli, such as faces and bodies. How the brain registers and interprets these stimuli, extracting both coarse and precise information about conspecifics and heterospecifics, is of great interest for understanding the visual brain, as well as for understanding how such processes are affected in certain psychiatric diseases. In the first study, we ask how neurons in IT acquire, maintain, and change their stimulus response selectivity over time. To this end, we developed a chronic recording array of inertialess microwires that were capable of following the activity of single neurons across multiple days. We first used this technique to demonstrate that, in the absence of explicit learning pressure, the pattern of visual responses evoked by large sets of stimuli is remarkably stable over periods of as long as one month. We then asked how the acquisition of new perceptual expertise affects the visual responses of IT neurons. Monkeys were trained to sort large stimulus sets into two different categories based on reward outcome. Learning altered the visual responses in 68% (21/31) of longitudinally recorded spiking responses. These changes included both activity increases and decreases, and in some cases lead to the genesis of new spiking responses to stimuli that were previously ineffective at driving the cell. Learning-related changes were also evident in the local field potential. Although the monkeys'behavior indicated that perceptual learning was essentially complete after a one hour training session, the learning-induced changes in IT visual responses did not emerge until 24 hours later. This delayed expression of neural plasticity indicates that changes in IT visual responses are a consequence of learning, rather than the causal driver of learning, and may reflect a process of memory consolidation. The second study investigates the functional layout of the ventral visual pathway of the common marmoset, testing responses to stimulus categories commonly tested in humans and macaques. In collaboration with Dr. Afonso Silva from NINDS, we have for the first time measured fMRI and electrocorticography responses in trained, behaving marmosets, and we describe a network of discrete face- and body-selective patches in the marmoset object pathway. Understanding the relationship of these patches to those commonly observed in in macaques and humans may shed new light on the principles of high-level category representation in the primate brain. The third study involves the measurement and decipherment of electrophysiological and fMRI signals in the macaque brain during the free viewing of natural videos. While natural viewing paradigms are, almost by definition, less controlled than conventional testing designs, they provide alternate and important perspectives on processing in brain areas such as IT. For example, we have shown that motion signals are, quite unexpectedly, the primary determinant of fMRI activity in the ventral object pathway. We have also found that while nearby neurons in a face patch all respond reliably to a natural movie, their reliable responses are nearly uncorrelated with one another. Neurons in the IT cortex respond to diverse types of complex stimuli, including natural categories such as faces or biological movement. Monkey electrophysiology experiments typically assess neural response selectivity by presenting multiple, short duration stimuli while the animal fixates a small point. The responses of a given neuron are typically evaluated over the course of an hour or two. Here we consider how IT neurons respond under more naturalistic viewing conditions, in which the animal freely views dynamic videos of conspecifics and heterospecifics in a range of social contexts. Using chronically implanted microwire arrays (Bondar et al, 2009), we further evaluate the extent to which neurons respond similarly to a video over much longer periods. Three rhesus macaques repeatedly viewed up to 12 different five-minute movies varying in social content. We collected spiking and broadband field potential responses from 32 and 64 channel microwire bundles chronically implanted in the lower bank and fundus of the superior temporal sulcus (STS). Analysis of gaze position revealed a high degree of overlap in fixation targets between viewings, and particularly those surrounding salient social events. Moreover, epochs of high and low spiking were strikingly consistent between multiple viewings of the same movie, even when they were not obviously linked to specific stimulus variables such as faces, bodies, or movement. Analysis of single units maintained over multiple sessions (up to four months) revealed that such consistency was also observed across different days and even over several weeks. Neural responses to individual events were robust to shuffling of the individual scenes at approximately 40 second long time scales. These results demonstrate that the repeated viewing approach provides a window into the role of individual neurons in the encoding of complex stimulus sequences, even under conditions in which the primary determinants of neural responsiveness cannot be summarized in terms identifiable high- or low-level stimulus features. These and other observations raise new questions about how our current experimental understanding of face and object representation in the ventral stream should be understood in the context of the brain's normal modes of operation.

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Russ, Brian E; Kaneko, Takaaki; Saleem, Kadharbatcha S et al. (2016) Distinct fMRI Responses to Self-Induced versus Stimulus Motion during Free Viewing in the Macaque. J Neurosci 36:9580-9
Miller, Cory T; Freiwald, Winrich A; Leopold, David A et al. (2016) Marmosets: A Neuroscientific Model of Human Social Behavior. Neuron 90:219-33
Murphy, Aidan P; Leopold, David A; Humphreys, Glyn W et al. (2016) Lesions to right posterior parietal cortex impair visual depth perception from disparity but not motion cues. Philos Trans R Soc Lond B Biol Sci 371:
Hung, ChiaChun; Day-Cooney, Julian; Russ, Brian et al. (2015) Neural responses to naturalistic movies in the common marmoset using electrocorticography and fMRI. J Vis 15:580
McMahon, David B T; Russ, Brian E; Elnaiem, Heba D et al. (2015) Single-unit activity during natural vision: diversity, consistency, and spatial sensitivity among AF face patch neurons. J Neurosci 35:5537-48
Hung, Chia-Chun; Yen, Cecil C; Ciuchta, Jennifer L et al. (2015) Functional mapping of face-selective regions in the extrastriate visual cortex of the marmoset. J Neurosci 35:1160-72
Dougherty, Kacie; Cox, Michele A; Ninomiya, Taihei et al. (2015) Ongoing Alpha Activity in V1 Regulates Visually Driven Spiking Responses. Cereb Cortex :
Russ, Brian E; Leopold, David A (2015) Functional MRI mapping of dynamic visual features during natural viewing in the macaque. Neuroimage 109:84-94
Mitchell, Jude F; Leopold, David A (2015) The marmoset monkey as a model for visual neuroscience. Neurosci Res 93:20-46
Izpisua Belmonte, Juan Carlos; Callaway, Edward M; Caddick, Sarah J et al. (2015) Brains, genes, and primates. Neuron 86:617-31

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