A combinatorial input landscape in the "higher-order relay" posterior thalamic nucleus

Each one of the many pathways that target the thalamus terminates directly onto the thalamic projection cells. As these cells lack excitatory interconnections, their computations are fundamentally defined by the type and local convergence of the extrinsic inputs. These two crucial input variables remain poorly defined for the “higher order relay” (HO) nuclei that constitute most of the thalamus in large-brained mammals, including humans. Here, we systematically analyzed the input landscape of a representative HO nucleus of the mouse thalamus, the posterior nucleus (Po). We examined the neuropil distribution of terminals immunopositive for markers of excitatory or inhibitory neurotransmission, mapped input sources across the brain and spinal cord and compared the intranuclear distribution and varicosity size of axons originated from each input source. Our findings reveal a complex landscape of partly overlapping input-specific microdomains. Cortical layer 5 afferents from somatosensory and motor areas predominate in central and ventral Po but are less abundant in other parts of the nucleus. Excitatory inputs from the trigeminal complex, dorsal column nuclei, spinal cord and superior colliculus as well as inhibitory terminals from anterior pretectal nucleus and zona incerta are each abundant in specific Po regions and absent from others. Cortical layer 6 and reticular thalamic nucleus terminals are evenly distributed across Po. Integration of specific input motifs by particular cell subpopulations may be commonplace within HO nuclei, and favor the emergence of computationally specialized input-output subnetworks.