713-348-4749 aaz@rice.edu

Large-scale recording of population activity during social cognition in freely moving non-human primates

Social interactions, a ubiquitous aspect of our everyday life, are critical to the health and survival of the species, but little is known about their underlying neural computations. The major limitation preventing our understanding of the neural underpinnings of social cognition is the lack of a suitable framework to allow us to study how it emerges in real time from interactions among brain networks. Indeed, examining the neural bases of complex social interactions has been traditionally performed by studying the brain of nonhuman primates in a laboratory environment in which the head and body are restrained while synthetic stimuli are presented on a computer monitor. However, it has become increasingly understood that studying the brain in spatially confined, artificial laboratory rigs poses severe limits on our capacity to understand the function of brain circuits. To overcome these limitations, we propose a novel approach to understand the neural underpinnings of social cognition. We will use a high-yield wireless system to study the cortical dynamics and plasticity of social interactions by recording population activity in multiple visual, temporal, and prefrontal cortical areas while nonhuman primates are interacting freely with their environment and with other animals. This new approach will enable us to uncover the dynamics of neuronal network activity that drives social interactions in an ethologically relevant behavioral task that involves sensory integration, memory, and complex decision-making. Our integrative project brings together innovative brain recording technologies and microelectronics together with large data sets analysis techniques. Our proposed research will constitute a paradigm shift by moving social neuroscience ? from simply observing animal behavior and recording the responses of single cells ? to a quantitative understanding of the distributed neuronal network encoding during social behavior in freely moving nonhuman primates performing rich naturalistic tasks. We anticipate that the large quantity of neural data recorded using our approach will be of great interest to clinicians and computational neuroscientists studying general properties of normal and dysfunctional neural networks, possibly leading to medical insights into the mechanisms of autism and attention deficit disorders that impair social interactions.

Large-scale recording of population activity during social cognition in freely moving non-human primates

a Schematic of wireless recording system from a 96-channel microelectrode array in dlPFC of freely behaving macaque. Array image photo credit: Utah Array—© 2020 Blackrock Microsystems, LLC. Monkey cartoon diagram image credit: Reproduced with permission35. © IOP Publishing. All rights reserved. Three-dimensional brain cartoon generated with Scaleable Brain Atlas36,37,38. b (Left) Schematic of wireless eye tracking system. (Right, top) Example of wirelessly recorded eye image with pupil detection. (Right, bottom) Example of wirelessly recorded pupil diameter. c Monkey movement is quantified based on consecutive video frames as the number of pixels that changed in intensity. The average movement during wakefulness for each recording session was used as a threshold to classify 10 s epochs as active or quiet wakefulness. (Top left and top middle) Example of two subsequent frames during quiet wakefulness, (top right) pixel-wise subtraction reveals no motion during this period. (Bottom left and bottom middle) Example of two subsequent frames during active wakefulness. (Bottom right) Pixel-wise subtraction reveals that the monkey is actively behaving during this period. d (top) Example raster showing the firing rates of 29 simultaneously recorded single units while the monkey is awake. The spike count in each 10 ms bin was converted to sp/s by scaling by a factor of 100. (Bottom) Population firing rate was computed as the average firing rate for the population within each 10 ms bin (black trace). The red line shows the average population firing rate for the whole 10 s period shown (6.3 sp/s). Population synchrony index (PSI) is 0.0433. PSI quantifies the 0.5–10 Hz oscillations of the population firing rate during the 10 s period. e Same as b, but recorded while the monkey is resting. Low-frequency fluctuations are apparent in both spike rasters and population firing rate. Average population firing rate is 4.5 sp/s and PSI is 0.0632.