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, D.C.W. Lo, Neda Khanjani, Bin Zhang, Jim Stanis, Ian Bowman, Kaelan Cotter, Chunru Cao, Seita Yamashita, Amanda J. Tugangui, Anan Li, Tao Jiang, Xueyan Jia, Zhao Feng, Sarvia Aquino, Hyun-Seung Mun, Muye Zhu, Anthony Santarelli, Nora L. Benavidez, Monica Y. 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 R. Wickersham, Qingming Luo, Joel D. Hahn, Byung Kook Lim, Li I. Zhang, Carlos Cepeda, Houri Hintiryan, Hong‐Wei Dong
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 associative 1–4 . 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 cortex 5 . 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.