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A large part of the thalamus is not directly involved in relaying ascending sensory inputs to the cerebral cortex. The functions and wiring of such “non-primary” nuclei remain unclear. The Posterior nucleus, a representative “non-primary” nucleus of the rodent thalamus, receives heavy and powerful inputs from cortical layer 5 (L5) cells. In addition, Po receives also some trigeminal, spinal and superior colliculus (SC) inputs, as well as powerful inhibitory inputs from the zona incerta (ZI) and anterior pretectal nucleus (APT). To elucidate to which extent these input systems converge or remain separate within Po, we first mapped the distribution of terminals immunolabeled for markers of glutamatergic or GABAergic neurotransmission and L5 terminals constitutively labeled in Rbp4-Cre;Ai14 mice. Besides, we retrogradely traced and quantified the sources of brain and spinal cord input reaching different Po regions. In addition, we compared bouton sizes in axons anterogradely labeled from the above input sources. Our data delineate several domains within Po, each dominated by specific sets of inputs. Cortical L5 afferents predominate in central and ventral Po. In contrast, large glutamatergic terminals from the trigeminal complex and spinal cord as well as GABAergic terminals from APT and ZI prevail in rostral and dorsal Po, and along the border with the ventral posteromedial nucleus. SC inputs preferentially target dorsal and caudal Po. These findings reveal multiple partly overlapping domains within Po. Hence, thalamic neuron subpopulations in different parts of Po may integrate diverse combinations of tactile, motor and pain-related inputs and give rise to functionally diverse thalamocortical subnetworks.

All pathways targeting the thalamus terminate directly onto the thalamic projection cells. As these cells lack local excitatory interconnections, their computations are fundamentally defined by the type and local convergence patterns of the extrinsic inputs. These two key variables, however, 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 in adult male and female mice 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 (L)5 afferents from somatosensory and motor areas predominate in central and ventral Po but are relatively less abundant in dorsal and lateral portions of the nucleus. Excitatory inputs from the trigeminal complex, dorsal column nuclei (DCN), spinal cord and superior colliculus as well as inhibitory terminals from anterior pretectal nucleus and zona incerta (ZI) are each abundant in specific Po regions and absent from others. Cortical L6 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 multiple, functionally diverse input-output subnetworks. SIGNIFICANCE STATEMENT Because thalamic projection neurons lack local interconnections, their output is essentially determined by the kind and convergence of the long-range inputs that they receive. Fragmentary evidence suggests that these parameters may vary within the “higher-order relay” (HO) nuclei that constitute much of the thalamus, but such variation has not been systematically analyzed. Here, we mapped the origin and local convergence of all the extrinsic inputs reaching the posterior nucleus (Po), a typical HO nucleus of the mouse thalamus by combining multiple neuropil labeling and axon tracing methods. We report a complex mosaic of partly overlapping input-specific domains within Po. Integration of different input motifs by specific cell subpopulations in HO nuclei may favor the emergence of multiple, computationally specialized thalamocortical subnetworks.