For nearly fifty years, systems neuroscientists have been discussing the existence of grandmother cells in the brain, referring to specialized neurons whose activity supports the recognition of individuals. Over the past several years, this notion has been rounded out within the broader field of social neuroscience. At present, we are in a phase of rapid learning about brain areas engaged during social perception. This research has a direct bearing on a wide range of patients, as social perceptual deficits are a hallmark of many psychiatric illnesses. Our recent research has asked how neurons in the high-level visual cortex respond to social stimuli presented in different contexts. Over the past year, we have extensively used a microwire bundle array developed and modified in our laboratory that is able to longitudinally track the activity of cells in the brain that reside in so-called face patches. Face patches are small, circumscribed regions of the temporal and prefrontal cortex showing greater fMRI responses to faces than to other categories of stimuli. The longitudinal nature of the recordings allows us to investigate individual neurons for weeks or months at a time. Since our early work established that neurons in these areas are remarkably stable in their responses, testing over this period means that we are able to examine how single cells respond to a very large array of artificial and natural stimuli and conditions. More recently, we have developed an avatar face stimulus, whose animation, facial expressions, and environmental context is under complete experimental control. This stimulus toolbox has been of great use for systematically studying the factors that determine neural firing, for example in the context of the geometry of natural vision. One is able through the variation of different stimulus dimensions, to determine whether internal facial features, external features of the head, shoulder and body, the angle of gaze, the illumination and setting, and a range of other factors influence the responses of cells that are nominally face-selective. In one recently completed study in the laboratory, we investigated how an internalized average face stored in the brain contributes to the determination of facial identity. This hypothesis, which fits together with the concept of norm-based encoding, posits that the brain responds to individual faces as deviations from an internally stored average prototype. We found strong evidence for norm-based tuning for morphed faces, which only arose after >200ms, long after the neurons initial response latency. Based on several observations, including measures of cell-to-cell activity coherence, we posit that this tuning is the product of late inhibition, whereby a subset of specialized neurons transmits broad inhibition to the population when the average norm face is shown. The discounting of average face information can be seen as a form of normalization that heightens the brains sensitivity to the distinguishing features of individual faces. We have also completed a study investigating the critical elements for driving neurons in the different face patches. One of the striking features of the study is the extent to which a very small region of a given face can determine the neuron's response, and the extent to which responses to this important feature are robust to major changes to the scene. For example, neurons responding selectively to one set of eyes often continue to respond to those eyes even when they are placed within a different face, which is attached to a different body and placed in a different scene. The local domination of such features was surprising, particularly as they were measured from the same neural populations as the norm-based coding findings mentioned above. We have also studied plasticity and learning in the responses of neurons in face patches. Notably, we found that face patches differ markedly in their capacity for plasticity, at least with respect to that associated with the basic familiarity of stimuli. Whereas the anterior fundus face patches show little if any response change across days and weeks, those in the anterior medial face patch show the selective elimination of late-phase activity that arises after several days. We are also investigating face selective regions using Ca++ fluorescence imaging and endoscopic lenses, and are now at the stage of collecting data. Similar to the microelectrode recordings, these recordings also give the capacity for longitudinal tracking over weeks and months. Thus, our Ca++ fluorescence work will also will be used to investigate whether neurons in face selective areas modify their response profiles as the subjects learn new faces.
| 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 |
Showing the most recent 10 out of 27 publications
