A frontal transcallosal inhibition loop mediates interhemispheric balance in visuospatial processing

Yanjie Wang, Zhaonan Chen, Guofen Ma, Lizhao Wang, Yanmei Liu, Meiling Qin, Xiang Fei, Yifan Wu, Min Xu () and Siyu Zhang ()
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Yanjie Wang: Shanghai Jiao Tong University, School of Medicine
Zhaonan Chen: Shanghai Jiao Tong University, School of Medicine
Guofen Ma: Shanghai Jiao Tong University, School of Medicine
Lizhao Wang: Shanghai Jiao Tong University, School of Medicine
Yanmei Liu: Shanghai Jiao Tong University, School of Medicine
Meiling Qin: Chinese Academy of Sciences
Xiang Fei: Chinese Academy of Sciences
Yifan Wu: Shanghai Jiao Tong University, School of Medicine
Min Xu: Chinese Academy of Sciences
Siyu Zhang: Shanghai Jiao Tong University, School of Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-21

Abstract: Abstract Interhemispheric communication through the corpus callosum is required for both sensory and cognitive processes. Impaired transcallosal inhibition causing interhemispheric imbalance is believed to underlie visuospatial bias after frontoparietal cortical damage, but the synaptic circuits involved remain largely unknown. Here, we show that lesions in the mouse anterior cingulate area (ACA) cause severe visuospatial bias mediated by a transcallosal inhibition loop. In a visual-change-detection task, ACA callosal-projection neurons (CPNs) were more active with contralateral visual field changes than with ipsilateral changes. Unilateral CPN inactivation impaired contralateral change detection but improved ipsilateral detection by altering interhemispheric interaction through callosal projections. CPNs strongly activated contralateral parvalbumin-positive (PV+) neurons, and callosal-input-driven PV+ neurons preferentially inhibited ipsilateral CPNs, thus mediating transcallosal inhibition. Unilateral PV+ neuron activation caused a similar behavioral bias to contralateral CPN activation and ipsilateral CPN inactivation, and bilateral PV+ neuron activation eliminated this bias. Notably, restoring interhemispheric balance by activating contralesional PV+ neurons significantly improved contralesional detection in ACA-lesioned animals. Thus, a frontal transcallosal inhibition loop comprising CPNs and callosal-input-driven PV+ neurons mediates interhemispheric balance in visuospatial processing, and enhancing contralesional transcallosal inhibition restores interhemispheric balance while also reversing lesion-induced bias.

Date: 2023
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DOI: 10.1038/s41467-023-40985-5

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