A Functional and Non-Homuncular Representation of the Larynx in the Primary Motor Cortex of Mice, a Vocal Non-Learner

Author:

Vargas César D. M.ORCID,Agravat Rajvi K.,Waidmann Elena N.ORCID,Bochalis Christodoulos,Bermudez Hector,Giannakopoulos TheodorosORCID,Jarvis Erich D.ORCID

Abstract

SummaryVocalization is a complex behavior ranging from fully innate to advanced vocal learning. Vocal learning species possess a vocal primary motor cortex (M1) region that makes direct projections to brainstem vocal motor neurons, which are thought to facilitate learning and fine modulation of vocalizations. Surprisingly, a similar, albeit sparse, direct projection from M1 was found in mice. Mice produce ultrasonic vocalizations (USV) which appear to be mostly innate. Modulation of these USVs is impacted by lesions to this M1 region, but genetic ablation of the cortex leads to few, if any, changes to USVs. It remained unclear whether M1 has any control over the vocal organ in a vocal non-learning species. In the current study, we found that stimulation in different parts of M1 in mice can generate contractions in laryngeal and jaw muscles, with different latencies suggestive of both direct and indirect projections to brainstem vocal motor neurons. Viral tracing reveals both single- and double-labeled populations of cortical neurons that simultaneously innervate laryngeal, jaw, and forelimb motor circuits. Chemical lesions reveal that an anterolateral orofacial region of M1 regulates the number of syllables in vocal sequences. Our results provide evidence that M1 in a vocal non-learner has some influence on vocal musculature, consistent with the continuum hypothesis of vocal learning. They also reveal that the representations of muscles for different behaviors across mouse M1 are more intermixed than previously considered. We discuss how these results impact hypotheses on the evolution of cortical vocal control and motor cortex organization.

Publisher

Cold Spring Harbor Laboratory

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