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Abstract

The ability to accurately determine when to perform an action is a fundamental brain function and vital to adaptive behavior. The behavioral mechanism and neural circuit for action timing, however, remain largely unknown. Using a new, self-paced action timing task in mice, we found that deprivation of auditory, but not somatosensory or visual input, disrupts learned action timing. The hearing effect was dependent on the auditory feedback derived from the animal’s own actions, rather than passive environmental cues. Neuronal activity in the secondary auditory cortex was found to be both correlated with and necessary for the proper execution of learned action timing. Closed-loop, action-dependent optogenetic stimulation of the specific task-related neuronal population within the secondary auditory cortex rescued the key features of learned action timing under auditory deprivation. These results unveil a previously underappreciated sensorimotor mechanism in which the secondary auditory cortex transduces self-generated audiomotor feedback to control action timing.

By applying operant conditioning, behavioral manipulation, in vivo electrophysiology, computational modeling, and closed-loop optogenetics, the authors reveal a mechanism for action timing in mice mediated by the secondary auditory cortex.

Details

Title
Secondary auditory cortex mediates a sensorimotor mechanism for action timing
Author
Cook, Jonathan R 1 ; Li, Hao 2   VIAFID ORCID Logo  ; Nguyen, Bella 2 ; Huang Hsiang-Hsuan 3 ; Mahdavian Payaam 2 ; Kirchgessner, Megan A 4   VIAFID ORCID Logo  ; Strassmann, Patrick 3 ; Engelhardt, Max 2 ; Callaway, Edward M 5   VIAFID ORCID Logo  ; Jin, Xin 6   VIAFID ORCID Logo 

 Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, USA (GRID:grid.250671.7) (ISNI:0000 0001 0662 7144); University of California, San Diego, Neurosciences Graduate Program, La Jolla, USA (GRID:grid.266100.3) (ISNI:0000 0001 2107 4242); Champalimaud Centre for the Unknown, Champalimaud Research, Champalimaud Foundation, Lisbon, Portugal (GRID:grid.421010.6) (ISNI:0000 0004 0453 9636) 
 Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, USA (GRID:grid.250671.7) (ISNI:0000 0001 0662 7144) 
 Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, USA (GRID:grid.250671.7) (ISNI:0000 0001 0662 7144); University of California, San Diego, Neurosciences Graduate Program, La Jolla, USA (GRID:grid.266100.3) (ISNI:0000 0001 2107 4242) 
 University of California, San Diego, Neurosciences Graduate Program, La Jolla, USA (GRID:grid.266100.3) (ISNI:0000 0001 2107 4242); Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, La Jolla, USA (GRID:grid.250671.7) (ISNI:0000 0001 0662 7144); New York University School of Medicine, Skirball Institute for Biomolecular Medicine, New York, USA (GRID:grid.137628.9) (ISNI:0000 0004 1936 8753) 
 Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, La Jolla, USA (GRID:grid.250671.7) (ISNI:0000 0001 0662 7144) 
 Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, USA (GRID:grid.250671.7) (ISNI:0000 0001 0662 7144); Center for Motor Control and Disease, Key Laboratory of Brain Functional Genomics, East China Normal University, Shanghai, China (GRID:grid.22069.3f) (ISNI:0000 0004 0369 6365); New York University Shanghai, NYU–ECNU Institute of Brain and Cognitive Science, Shanghai, China (GRID:grid.449457.f) (ISNI:0000 0004 5376 0118) 
Pages
330-344
Publication year
2022
Publication date
Mar 2022
Publisher
Nature Publishing Group
ISSN
10976256
e-ISSN
15461726
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
2637587810
Copyright
© The Author(s), under exclusive licence to Springer Nature America, Inc. 2022.