Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations

Abstract

Broca's area in the ventrolateral prefrontal cortex (vlPFC) has a crucial role in human volitional speech production; damage to this area causes severe impairment of speech production. Lesions in PFC of monkeys, however, have only mild effects on spontaneous vocal behaviour. Non-human primate vocalizations are thus believed to constitute affective utterances processed by a subcortical network. Here in contrast to this assumption, we show that rhesus monkeys can control their vocalizations in a goal-directed way. During single-cell recordings in the vlPFC of monkeys trained to vocalize in response to visual cues, we find call-related neurons that specifically predict the preparation of instructed vocalizations. The activity of many call-related neurons before vocal output correlates with call parameters of instructed vocalizations. These findings suggest a cardinal role of the monkey homologue of Broca's area in vocal planning and call initiation, a putative phylogenetic precursor in non-human primates for speech control in linguistic humans.

Responses of primate frontal cortex neurons during natural vocal communication

“…The neurophysiological properties of vocal motor-responsive neurons in the current experiment contrast with recent studies of trained vocal production in rhesus monkeys (Coude et al 2011;Hage and Nieder 2013). Similarly to these rhesus monkey experiments, we found that neurons in ventral prefrontal area 44/45, putative Broca's homolog, and ventral premotor cortex exhibit vocal motor-related changes in activity.…”

“…This suggests that while individual neurons were not driven by vocalization stimuli in this natural behavior, these populations do play some role in communication signal processing. Potential explanations for the observed differences between earlier studies of vocalization processing (Romanski and Averbeck 2009) and vocal-motor production (Coude et al 2011;Hage and Nieder 2013) in restrained primates and data reported here during natural communication are discussed below. These data provide a foundation for future neurophysiological experiments and are suggestive that implementing more naturalistic behavioral paradigms are important for elucidating the neural basis of NHP vocal communication.…”

“…However, since similar effects with microstimulation in PAG and lesions to frontal cortex have been reported in humans (Jurgens 2002;Kertesz and McCabe 1977), the involvement of subcortical motor nuclei for vocal production does not preclude a role for frontal cortex. In fact, several recent experiments suggest that frontal cortex may contribute to some aspects of vocal production (Coude et al 2011;Gemba et al 1999;Hage and Nieder 2013;Miller et al 2010a;Simoes et al 2010). Microstimulation of ventrolateral prefrontal cortex area 44 in rhesus monkeys, for example, results in orofacial movements (Petrides et al 2005).…”

Abstract rule neurons in the endbrain support intelligent behaviour in corvid songbirds

“…Both NCL and PFC are multimodal association areas that operate at the top of the telencephalicprocessing hierarchy 16,41 , ideally positioned to integrate sensory input and project to motor output 15 . Posterior movementassociated areas, such as the NCL, have been suggested to show activity related to movements and vocalizations 42 , again reflecting PFC function 43,44 . Moreover, like the PFC, the NCL is densely innervated by dopaminergic fibres from the midbrain 35,36,45 .…”

A comparative neurological approach to emotional expressions in primate vocalizations

“…anterior cingulate gyrus) in monkeys have been connected to the learning of vocalizations in particular foodbased paradigms (Gemba et al, 1995), whether they are truly connected to the voluntary characteristic of vocal production or instead to the motivation to obtain the food reward remains unclear (Aboitiz et al, 2006;Liebal et al, 2014). More recent findings suggest that neurons in the prefrontal cortex mediate voluntary vocalizations in monkeys (Coudé et al, 2011;Hage and Nieder, 2013) although this control may disappear with age suggesting a different evolutionary pathway compared to humans (Hage et al, 2016).…”