Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain

• Type of Material: Article
• Authors: James N McGregor, Emory University; Abigail L Grassler, Emory University; Paul I Jaffe, University of California, San Francisco; Amanda L Jacob, Emory University; Michael S Brainard, University of California, San Francisco; Samuel Sober, Emory University
• Language: English
• Date: 2022-09-01
• Publisher: eLife Sciences Publications Ltd
• Publication Version: Final Published Version
• Copyright Statement: © 2022, McGregor, Grassler et al
• Final Published Version (URL): http://dx.doi.org/10.7554/eLife.75691
• Title of Journal or Parent Work: eLife
• Volume: 11
• Grant/Funding Information: Howard Hughes Medical Institute to Paul I Jaffe, Michael S Brainard.; National Institutes of Health R01-NS084844 to James N McGregor.; Simons Foundation Emory International Consortium on Motor Control to Samuel J Sober.; National Institutes of Health R01-EB022872 to James N McGregor.; National Institutes of Health R01-NS099375 to James N McGregor.; This paper was supported by the following grants:
• Keywords: songbird; neuroscience; Feedback, Sensory; Bengalese finch; Songbirds; Basal Ganglia; Humans; Finches; Learning; Vocalization, Animal; lonchura striata var. domestica; Animals
• Research Categories: Biology, General

Abstract

Songbirds and humans share the ability to adaptively modify their vocalizations based on sensory feedback. Prior studies have focused primarily on the role that auditory feedback plays in shaping vocal output throughout life. In contrast, it is unclear how non-auditory information drives vocal plasticity. Here, we first used a reinforcement learning paradigm to establish that somato-sensory feedback (cutaneous electrical stimulation) can drive vocal learning in adult songbirds. We then assessed the role of a songbird basal ganglia thalamocortical pathway critical to auditory vocal learning in this novel form of vocal plasticity. We found that both this circuit and its dopaminergic inputs are necessary for non-auditory vocal learning, demonstrating that this pathway is critical for guiding adaptive vocal changes based on both auditory and somatosensory signals. The ability of this circuit to use both auditory and somatosensory information to guide vocal learning may reflect a general principle for the neural systems that support vocal plasticity across species.