Genoarchitecture and input-output organization of the mouse basal ganglia and thalamic parafascicular nucleus.

The basal ganglia comprise interconnected subcortical nuclei essential for motor control, learning, emotion and cognition, yet how cell types relate to their circuit organization remains elusive. Here we show that spatial patterns of transcriptomic cell types in the basal ganglia and thalamic parafascicular nucleus relate to module-organized cortical inputs in the mouse. By co-registering genoarchitectural and connectivity datasets to the common coordinate framework, we delineate distinct three-dimensional subdivisions of these nuclei. Analyses of anterograde and retrograde viral tracing data and single-neuron reconstructions reveal that each subdivision receives convergent, modular and cell-type-specific cortical and subcortical inputs. Caudoputamen subdivisions primarily receive layer 5 intratelencephalic inputs from the entire isocortex, whereas smaller basal ganglia subdivisions receive ipsilateral layer 5 extratelencephalic inputs from limited cortical areas. The parafascicular nucleus subdivisions are connected with specific cortical modules and basal ganglia subdivisions. Our results suggest that combinatorial gene expression underlies a global map of parallel, modular and cell-type-specific basal ganglia and parafascicular nucleus subnetworks.