Social Context-Dependent Activity in Marmoset Frontal Cortex Populations during Natural Conversations

Abstract

Communication is an inherently interactive process that weaves together the fabric of both human and nonhuman primate societies. To investigate the properties of the primate brain during active social signaling, we recorded the responses of frontal cortex neurons as freely moving marmosets engaged in conversational exchanges with a visually occluded virtual marmoset. We found that small changes in firing rate (ϳ1 Hz) occurred across a broadly distributed population of frontal cortex neurons when marmosets heard a conspecific vocalization, and that these changes corresponded to subjects' likelihood of producing or withholding a vocal reply. Although the contributions of individual neurons were relatively small, large populations of neurons were able to clearly distinguish between these social contexts. Most significantly, this social context-dependent change in firing rate was evident even before subjects heard the vocalization, indicating that the probability of a conversational exchange was determined by the state of the frontal cortex at the time a vocalization was heard, and not by a decision driven by acoustic characteristics of the vocalization. We found that changes in neural activity scaled with the length of the conversation, with greater changes in firing rate evident for longer conversations. These data reveal specific and important facets of this neural activity that constrain its possible roles in active social signaling, and we hypothesize that the close coupling between frontal cortex activity and this natural, active primate social-signaling behavior facilitates social-monitoring mechanisms critical to conversational exchanges.

Internal states and extrinsic factors both determine monkey vocal production

“…In primates (including humans), vocalizations are produced via the coordination of brain regions within a "medial" pathway involved in both arousal regulation and the motor aspects of vocal production and a "lateral" pathway that is involved in volitional control of vocal production through learning (11,43). Recent neurophysiological data are consistent with these ideas [macaque monkeys (44,45); marmosets (46)(47)(48)].…”

Functional magnetic resonance imaging of auditory cortical fields in awake marmosets

“…Similarly to recent fMRI experiments in marmoset vision (Hung et al, 2015a; Hung et al, 2015b) and somatosensory cortex (Yen et al, 2017), this preparation is amenable to techniques involving conditioned behavior and can, therefore, be extended to investigate relative contributions of multiple auditory cortical fields during behaviorally-dependent facets of audition (Remington et al, 2012; Song et al, 2016). Given the significance of marmosets as a neurobiological model of communication (Toarmino et al, 2017; Eliades & Wang, 2008; Miller et al, 2015; Eliades & Miller 2016; Miller, 2017; Nummela et al 2017), our approach could be implemented to identify areas of the auditory cortical system involved in vocalization processing (e.g., Sadagopan et al, 2015; Perrodin et al, 2011). Together, these approaches can shed light on auditory function in ways not previously possible.…”

Flexible usage and social function in primate vocalizations

“…It is well known, for example, that primate control of vocalization during operant conditioning is mediated by activity in the mediofrontal cortex, including the anterior cingulate gyrus (66). More recently, studies of marmosets (Callithrix jacchus) have examined the neural mechanisms underlying vocal exchanges between male and female partners (91)(92)(93). They provide evidence that a listener's decision to answer a call or remain silent can be predicted by changes in the firing rate of frontal cortex neurons even before an individual's partner has given a call.…”

“…They provide evidence that a listener's decision to answer a call or remain silent can be predicted by changes in the firing rate of frontal cortex neurons even before an individual's partner has given a call. This premotor activity occurs in both the frontal and the auditory cortex (93)(94)(95). It appears to be neither sensory-nor motor-driven, but instead depends upon the social context, constituting a "social monitoring mechanism critical to conversational exchanges" (93, p. 1,036).…”