Auditory representation of learned sound sequences in motor regions of the macaque brain

Abstract

<jats:p>Human speech production requires the ability to couple motor actions with their auditory consequences. Nonhuman primates might not have speech because they lack this ability. To address this question, we trained macaques to perform an auditory–motor task producing sound sequences via hand presses on a newly designed device (“monkey piano”). Catch trials were interspersed to ascertain the monkeys were listening to the sounds they produced. Functional MRI was then used to map brain activity while the animals listened attentively to the sound sequences they had learned to produce and to two control sequences, which were either completely unfamiliar or familiar through passive exposure only. All sounds activated auditory midbrain and cortex, but listening to the sequences that were learned by self-production additionally activated the putamen and the hand and arm regions of motor cortex. These results indicate that, in principle, monkeys are capable of forming internal models linking sound perception and production in motor regions of the brain, so this ability is not special to speech in humans. However, the coupling of sounds and actions in nonhuman primates (and the availability of an internal model supporting it) seems not to extend to the upper vocal tract, that is, the supralaryngeal articulators, which are key for the production of speech sounds in humans. The origin of speech may have required the evolution of a “command apparatus” similar to the control of the hand, which was crucial for the evolution of tool use.</jats:p>

Auditory Decisions in the Supplementary Motor Area

“…Furthermore, this is the first description of how SMA neuronal activity correlates with decisions based on active listening to naturalistic sounds. Interestingly, a small group of neurons coded for sounds during auditory periods, as predicted by imaging studies that suggested that the premotor cortex is activated by auditory stimuli (Lima et al, 2016;Vergara et al, 2016;Archakov et al, 2020). Nevertheless, to our knowledge, our results constitute the first electrophysiological evidence of SMA coding natural sounds.…”

“…In primates, auditory information is carried from the auditory cortex to the prefrontal and premotor cortices via ventral and dorsal auditory streams (Romanski et al, 1999;Kusmierek & Rauschecker, 2014). Recent studies with macaques have shown that premotor regions may represent an embodiment of acoustic recognitions (Archakov et al, 2020). The premotor supplementary motor area (SMA) has been linked to voluntary action and cognitive control of movement (Nachev et al, 2008;Lara et al, 2018;Shima & Tanji, 2000).…”

Putting Cells in Motion: Advantages of Endogenous Boosting of BDNF Production

“…Such response could be congenital, being observed in young children [ 24 ], and seems specifically human or at least restricted to vocal learning species, being seen only in rare instances such as in parrots or sea lions, apart from humans [ 25 ]. In addition to that, when we learn a song well or when we learn to play an instrument, the action observation brain network activates in humans [ 26 ], and also in primates [ 27 ]. In this commentary, we argue for the relevance of music for neurotrophic-mediated processes.…”

Reorganization of the neurobiology of language after sentence overlearning

“…These collectively show that perception after learning involves more engagement of the production systems used during learning. For example, in both monkeys and humans, learning to play sounds on a keyboard is subsequently associated with specific activation of sensorimotor regions involved in making finger and hand movements when listening to those sounds [80][81][82][83][84][85] . More generally, musical training improves sound and speech perception and these improvements are typically associated with sensorimotor regions [85][86][87][88][89][90] .…”