Neural signatures of natural behavior in socializing macaques

Abstract

Our understanding of the neurobiology of primate behavior largely derives from artificial tasks in highly-controlled laboratory settings, overlooking most natural behaviors primate brains evolved to produce1. In particular, how primates navigate the multidimensional social relationships that structure daily life and shape survival and reproductive success remains largely unexplored at the single neuron level. Here, we combine ethological analysis with new wireless recording technologies to uncover neural signatures of natural behavior in unrestrained, socially interacting pairs of rhesus macaques within a larger colony. Population decoding of single neuron activity in prefrontal and temporal cortex unveiled robust encoding of 24 species-typical behaviors, which was strongly modulated by the presence and identity of surrounding monkeys. Male-female partners demonstrated near-perfect reciprocity in grooming, a key behavioral mechanism supporting friendships and alliances, and neural activity maintained a running account of these social investments. When confronted with an aggressive intruder, behavioral and neural population responses reflected empathy and were buffered by the presence of a partner. Surprisingly, neural signatures in prefrontal and temporal cortex were largely indistinguishable and irreducible to visual and motor contingencies. By employing an ethological approach to the study of primate neurobiology, we reveal a highly-distributed neurophysiological record of social dynamics, a potential computational foundation supporting communal life in primate societies, including our own.

Hierarchical action encoding in prefrontal cortex of freely moving macaques

“…Some recent work has begun to unravel the neural processes that occur during free movement. 16 – 18 , 54 Our work builds on this past work in several ways. First, we were able to measure neural correlates of actions in an animal with a richer behavioral repertoire (59 distinct actions).…”

“…Currently, constructing an ethogram requires the delineation of ethogrammatical categories, which involves the time-consuming and careful annotation of behavior by highly trained human observers. 54 Human-led ethogramming is slow, extremely costly, error prone, and susceptible to characteristic biases. 61 – 64 For these reasons, it is simply impractical for even moderately large datasets, collected either in an open environment or in the home cage.…”

Representing the dynamics of natural marmoset vocal behaviors in frontal cortex

“…Perspectives on the neural basis of primate behavior are evolving in hand with the increased use of ethological paradigms 22,26,28,34,35 and particularly as effects in conventional tasks are not necessarily recapitulated in the presumptive analogous natural behaviors 15,32 . Our results here showed that -while functional clusters of these processes are evident in the prefrontal and premotor cortices of marmosets engaged in natural vocal interactions -the organization is widely distributed throughout frontal cortex; a stark contrast to the most directly analogous studies with conventional paradigms 29,30,32 .…”

“…Our results here showed that -while functional clusters of these processes are evident in the prefrontal and premotor cortices of marmosets engaged in natural vocal interactions -the organization is widely distributed throughout frontal cortex; a stark contrast to the most directly analogous studies with conventional paradigms 29,30,32 . We conjecture that the distributed functional organization during natural marmoset conversations was evident because the behavioral and cognitive processes that have traditionally been studied selectively through more targeted experimentation become more covaried in continuous, natural behaviors and, as such, rely on a more distributed computational ensemble coding strategy in primate frontal cortex 22 . Though admittedly limited in number, the few studies to directly compare neural responses in the primate brain between conventional and naturalistic paradigms have reported considerable differences 15,32 that may portend the need to evolve our conceptions of brain computations and behavior.…”

“…One potential explanation may be that changes in the state of frontal cortex during natural behaviors 5,7 or the inherent variability of ethological behaviors 1,4 may mask the subfield specializations evident in more conventional paradigms. Alternatively, features of natural behaviors -such as the occurrence of varying sequential events 1 -may drive distinct patterns of neural activity that do not emerge in more focused behavioral tasks 22 . To reconcile these issues, a more refined analysis approach that better accounts for these factors may be needed to characterize patterns of primate frontal cortex activity in natural, ethological behaviors.…”