Our social world is comprised of complex stimuli, relationships, rules, and emotions. Thus the social circuitry in the primate brain is a widespread set of regions that touches on each of these operations. Some of these subregions appear highly specialized, such as the multiple cortical areas in humans and nonhuman primates that contain neurons selectively responsive to faces. Learning is a vital element for effectively applying experiences in the social world. Following an encounter with an individual, it is critical to recall not only their identity, but how they appeared, the actions they took, and the feelings they evoked. Primates live in a complex and dynamic hierarchy in which the brain constantly needs to update its knowledge about others. This updating process necessarily hinges on the adjustment of neural synaptic strengths. How and where such plasticity takes place is largely unknown. Would, for example, newly acquired familiarity with a face be reflected in the selectivity of face-selective neurons in fMRI-defined face patches? We have recently employed a microwire bundle array developed in the laboratory to systematically follow the activity of neurons over much longer time scales than was previously possible. Several ongoing projects in the laboratory have used this approach to address questions related to the processing of social stimuli, as well as the extent to which neural responses change with experience. In the past year, we have performed several studies using these electrodes. In one such study (McMahon et al. J Neurosci (2015)), we used the microwire bundle arrays to track responses to the content of socially rich videos. In being able to study individual neurons for several weeks, we came to the surprising conclusion that a population of neurons that are all nominally face cells (in that they respond more to faces than to other visual objects), are almost completely decorrelated in their responses upon viewing naturalistic stimuli. In trying to understand this result, we developed a novel method by which the responses of individual neurons could be compared with the fMRI activity throughout the brain, such that each individual neuron gave rise to a functional MRI map. This study, which is on the verge of submission (Park, SH et al (2016), in preparation), demonstrates that there are distinct and intermixed subgroups of neurons within a single cubic millimeter of cortex in an fMRI-defined face patch. These subgroups are affiliated in their activity with vastly different brain networks, only a subset of which appear related to activity in other face patches. In another study (Jones et al (2016), in preparation), we have used these electrodes to measure the principles by which face-selective neurons encode individual identity. Specifically, we have shown that in two fMRI-face patches, respectively known as AF and AM, neurons respond with reference to an implicitly encoded norm, which is the average of all known faces. These findings support much psychophysical work suggesting that face identity processing is an inherently comparative process, with incoming faces judged according to their deviation from an internally stored prototype. In a recent collaborative review, we have recently highlighted the nature of high-level visual specialization in primates from a comparative neurological perspective (Leopold, Mitchell, and Freiwald, 2016, in press). In another thread of research, we have continued to use marmosets to study aspects of neural processing related to social stimuli. The marmoset is an up-and-coming animal model that has gained momentum recently owing to many experimental advantages. In a recent review article (Miller et al. (2016) Neuron), we have highlighted the multiple ways in which the marmoset model provides new avenues for studying the neural mechanisms of social interaction. We are presently planning collaborative experiments to investigate the brain under conditions of social interaction, such as when the neural activity and position of multiple, interacting animals is tracked. Of principle interest is the decision-making of individual animals within the context of their complex social groups.
| Mundinano, Inaki-Carril; Fox, Dylan M; Kwan, William C et al. (2018) Transient visual pathway critical for normal development of primate grasping behavior. Proc Natl Acad Sci U S A 115:1364-1369 |
| Dougherty, Kacie; Cox, Michele A; Ninomiya, Taihei et al. (2017) Ongoing Alpha Activity in V1 Regulates Visually Driven Spiking Responses. Cereb Cortex 27:1113-1124 |
| Toarmino, Camille R; Yen, Cecil C C; Papoti, Daniel et al. (2017) Functional magnetic resonance imaging of auditory cortical fields in awake marmosets. Neuroimage 162:86-92 |
| Taubert, Jessica; Wardle, Susan G; Flessert, Molly et al. (2017) Face Pareidolia in the Rhesus Monkey. Curr Biol 27:2505-2509.e2 |
| Park, Soo Hyun; Russ, Brian E; McMahon, David B T et al. (2017) Functional Subpopulations of Neurons in a Macaque Face Patch Revealed by Single-Unit fMRI Mapping. Neuron 95:971-981.e5 |
| Leopold, David A; Russ, Brian E (2017) Human Neurophysiology: Sampling the Perceptual World. Curr Biol 27:R71-R73 |
| 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 |
| 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: |
| Kaskan, P M; Costa, V D; Eaton, H P et al. (2016) Learned Value Shapes Responses to Objects in Frontal and Ventral Stream Networks in Macaque Monkeys. Cereb Cortex : |
| Miller, Cory T; Freiwald, Winrich A; Leopold, David A et al. (2016) Marmosets: A Neuroscientific Model of Human Social Behavior. Neuron 90:219-33 |
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