Behavioral context affects social signal representations within single primate prefrontal cortex neurons

Abstract

SummaryWe tested whether social signal processing in more traditional, head-restrained contexts is representative of the putative natural analog – social communication – by comparing responses to vocalizations within individual neurons in marmoset prefrontal cortex (PFC) across a series of behavioral contexts ranging from traditional to naturalistic. Although vocalization responsive neurons were evident in all contexts, cross-context consistency was notably limited. A response to these social signals when subjects were head-restrained was not predictive of a comparable neural response to the identical vocalizations during natural communication, even within the same neuron. Neural activity at the population level followed a similar pattern, as PFC activity could be reliably decoded for the context in which vocalizations were heard. This suggests that neural representations of social signals in primate PFC are not static, but highly flexible and likely reflect how nuances of the dynamic behavioral contexts affect the perception of these signals and what they communicate.

A vocalization-processing network in marmosets

“…While these regions have been proposed to play important roles in the cognitive control of vocalizations in primates (37), we did not observe any signs of vocalizations during the fMRI experiments. Although it is possible that these activations are related to movements of the ears or attempted head movements in response to the conspecific calls, it has also been shown that listening to conspecific calls activates neurons in areas 8AD, 8aV (22) and areas 6DR, 6DC, and 6M (38) in marmosets. In addition, human studies have reported activity in primary motor cortex that was activated and correlated with temporal voice patches during a listening task (39).…”

“…The marmoset auditory system has also been well-characterized making them ideal for studying the processing of vocalization (18). Single unit recordings have demonstrated vocalization-selective responses in marmoset auditory (19)(20)(21) and frontal cortices (22,23) and an fMRI study has reported vocalization-selective activation in the anterior temporal pole in anesthetized marmosets (24). Here, we took advantage of our recently developed radiofrequency (RF) coil and restraint system for ultrahigh field (9.4 Tesla) fMRI in awake marmosets (25) and acquired whole-brain fMRI while monkeys were presented with conspecific vocalizations, scrambled vocalizations, and nonvocal sounds.…”

A context-dependent switch from sensing to feeling in the primate amygdala

“…Indeed, in different cognitive contexts, neurons in various brain areas respond differentially to the same visual stimuli (Rainer et al, 1998; Mante et al, 2013; Saez et al, 2015). Recently Jovanovic and colleagues (2022) showed that the baseline firing rates of prefrontal neurons in marmosets appear to signal social context. Our finding of persistent changes in baseline activity linked to social context is consistent with those findings.…”

Orbitofrontal cortex populations are differentially recruited to support actions

“…We next sought to investigate whether OFC may reflect the use of such experiential information during decision-making, particularly lever press duration information. As head fixation can have large effects on context-dependent behaviors, 76 we monitored OFC population Ca 2+ activity of CaMKII+ projection populations (rAAV5/PAAV-CaMKIIa-GCaMP6s) using in vivo fiber photometry in freely-moving mice (C57BL/6J, n = 9 mice, 6 males, 3 females) as they performed the lever-press hold down task during 1600 ms duration criterion training (Figures 2A and S2). A perievent histogram of Ca 2+ traces ordered by press duration revealed that CaMKII+ OFC projection population activity was modulated at select epochs relative to lever press initiation and execution (Figure 2B).…”