Cingulate-motor circuits update rule representations for sequential choice decisions

Daigo Takeuchi, Dheeraj Roy, Shruti Muralidhar, Takashi Kawai, Andrea Bari, Chanel Lovett, Heather A. Sullivan, Ian R. Wickersham and Susumu Tonegawa ()
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Daigo Takeuchi: RIKEN-MIT Laboratory for Neural Circuit Genetics at the Picower Institute for Learning and Memory
Dheeraj Roy: RIKEN-MIT Laboratory for Neural Circuit Genetics at the Picower Institute for Learning and Memory
Shruti Muralidhar: RIKEN-MIT Laboratory for Neural Circuit Genetics at the Picower Institute for Learning and Memory
Takashi Kawai: RIKEN-MIT Laboratory for Neural Circuit Genetics at the Picower Institute for Learning and Memory
Andrea Bari: RIKEN-MIT Laboratory for Neural Circuit Genetics at the Picower Institute for Learning and Memory
Chanel Lovett: Howard Hughes Medical Institute, MIT
Heather A. Sullivan: McGovern Institute for Brain Research at MIT
Ian R. Wickersham: McGovern Institute for Brain Research at MIT
Susumu Tonegawa: RIKEN-MIT Laboratory for Neural Circuit Genetics at the Picower Institute for Learning and Memory

Nature Communications, 2022, vol. 13, issue 1, 1-19

Abstract: Abstract Anterior cingulate cortex mediates the flexible updating of an animal’s choice responses upon rule changes in the environment. However, how anterior cingulate cortex entrains motor cortex to reorganize rule representations and generate required motor outputs remains unclear. Here, we demonstrate that chemogenetic silencing of the terminal projections of cingulate cortical neurons in secondary motor cortex in the rat disrupts choice performance in trials immediately following rule switches, suggesting that these inputs are necessary to update rule representations for choice decisions stored in the motor cortex. Indeed, the silencing of cingulate cortex decreases rule selectivity of secondary motor cortical neurons. Furthermore, optogenetic silencing of cingulate cortical neurons that is temporally targeted to error trials immediately after rule switches exacerbates errors in the following trials. These results suggest that cingulate cortex monitors behavioral errors and updates rule representations in motor cortex, revealing a critical role for cingulate-motor circuits in adaptive choice behaviors.

Date: 2022
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DOI: 10.1038/s41467-022-32142-1

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