The mouse cortico–basal ganglia–thalamic network

Nicholas N. Foster (), Joshua Barry, Laura Korobkova, Luis Garcia, Lei Gao, Marlene Becerra, Yasmine Sherafat, Bo Peng, Xiangning Li, Jun-Hyeok Choi, Lin Gou, Brian Zingg, Sana Azam, Darrick Lo, Neda Khanjani, Bin Zhang, Jim Stanis, Ian Bowman, Kaelan Cotter, Chunru Cao, Seita Yamashita, Amanda Tugangui, Anan Li, Tao Jiang, Xueyan Jia, Zhao Feng, Sarvia Aquino, Hyun-Seung Mun, Muye Zhu, Anthony Santarelli, Nora L. Benavidez, Monica Song, Gordon Dan, Marina Fayzullina, Sarah Ustrell, Tyler Boesen, David L. Johnson, Hanpeng Xu, Michael S. Bienkowski, X. William Yang, Hui Gong, Michael S. Levine, Ian Wickersham, Qingming Luo, Joel D. Hahn, Byung Kook Lim, Li I. Zhang, Carlos Cepeda, Houri Hintiryan and Hong-Wei Dong ()
Additional contact information
Nicholas N. Foster: David Geffen School of Medicine at UCLA
Joshua Barry: David Geffen School of Medicine at UCLA
Laura Korobkova: University of Southern California
Luis Garcia: David Geffen School of Medicine at UCLA
Lei Gao: David Geffen School of Medicine at UCLA
Marlene Becerra: University of Southern California
Yasmine Sherafat: University of Southern California
Bo Peng: University of Southern California
Xiangning Li: Huazhong University of Science and Technology
Jun-Hyeok Choi: University of California, San Diego
Lin Gou: David Geffen School of Medicine at UCLA
Brian Zingg: David Geffen School of Medicine at UCLA
Sana Azam: University of Southern California
Darrick Lo: David Geffen School of Medicine at UCLA
Neda Khanjani: University of Southern California
Bin Zhang: David Geffen School of Medicine at UCLA
Jim Stanis: University of Southern California
Ian Bowman: David Geffen School of Medicine at UCLA
Kaelan Cotter: University of Southern California
Chunru Cao: David Geffen School of Medicine at UCLA
Seita Yamashita: David Geffen School of Medicine at UCLA
Amanda Tugangui: David Geffen School of Medicine at UCLA
Anan Li: Huazhong University of Science and Technology
Tao Jiang: JITRI Institute for Brainsmatics
Xueyan Jia: JITRI Institute for Brainsmatics
Zhao Feng: JITRI Institute for Brainsmatics
Sarvia Aquino: University of Southern California
Hyun-Seung Mun: David Geffen School of Medicine at UCLA
Muye Zhu: David Geffen School of Medicine at UCLA
Anthony Santarelli: University of Southern California
Nora L. Benavidez: David Geffen School of Medicine at UCLA
Monica Song: David Geffen School of Medicine at UCLA
Gordon Dan: University of Southern California
Marina Fayzullina: David Geffen School of Medicine at UCLA
Sarah Ustrell: University of Southern California
Tyler Boesen: David Geffen School of Medicine at UCLA
David L. Johnson: University of Southern California
Hanpeng Xu: David Geffen School of Medicine at UCLA
Michael S. Bienkowski: University of Southern California
X. William Yang: David Geffen School of Medicine at UCLA
Hui Gong: Huazhong University of Science and Technology
Michael S. Levine: David Geffen School of Medicine at UCLA
Ian Wickersham: Massachusetts Institute of Technology
Qingming Luo: Huazhong University of Science and Technology
Joel D. Hahn: University of Southern California
Byung Kook Lim: University of California, San Diego
Li I. Zhang: University of Southern California
Carlos Cepeda: David Geffen School of Medicine at UCLA
Houri Hintiryan: David Geffen School of Medicine at UCLA
Hong-Wei Dong: David Geffen School of Medicine at UCLA

Nature, 2021, vol. 598, issue 7879, 188-194

Abstract: Abstract The cortico–basal ganglia–thalamo–cortical loop is one of the fundamental network motifs in the brain. Revealing its structural and functional organization is critical to understanding cognition, sensorimotor behaviour, and the natural history of many neurological and neuropsychiatric disorders. Classically, this network is conceptualized to contain three information channels: motor, limbic and associative1–4. Yet this three-channel view cannot explain the myriad functions of the basal ganglia. We previously subdivided the dorsal striatum into 29 functional domains on the basis of the topography of inputs from the entire cortex5. Here we map the multi-synaptic output pathways of these striatal domains through the globus pallidus external part (GPe), substantia nigra reticular part (SNr), thalamic nuclei and cortex. Accordingly, we identify 14 SNr and 36 GPe domains and a direct cortico-SNr projection. The striatonigral direct pathway displays a greater convergence of striatal inputs than the more parallel striatopallidal indirect pathway, although direct and indirect pathways originating from the same striatal domain ultimately converge onto the same postsynaptic SNr neurons. Following the SNr outputs, we delineate six domains in the parafascicular and ventromedial thalamic nuclei. Subsequently, we identify six parallel cortico–basal ganglia–thalamic subnetworks that sequentially transduce specific subsets of cortical information through every elemental node of the cortico–basal ganglia–thalamic loop. Thalamic domains relay this output back to the originating corticostriatal neurons of each subnetwork in a bona fide closed loop.

Date: 2021
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DOI: 10.1038/s41586-021-03993-3

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