While both systems are used for active sensing, they differ in fundamental ways, ranging from the structure and function of the sensors (actively whisked vibrissal hairs versus glabrous pads and hairy skin) and proprioceptive systems (muscle spindles present in forelimb but largely absent in vibrissal musculature) ( Moore et al., 2015 Severson et al., 2019) to the modes of operation (bilaterally coupled oscillatory whisking versus diverse forelimb movements for manipulation and locomotion). Similar to the hand-related pathways, the ascending somatosensory pathways in this system include lemniscal and corticocortical pathways traversing the ventral posterior medial (VPM) nucleus, whisker S1, and whisker M1 additionally, however, a paralemniscal pathway conveys whisking-related signals via the posterior (PO) nucleus. In contrast, much is known about the circuit connections and structure-function relationships in corresponding transcortical pathways in the whisker-barrel system of rats and mice ( Feldmeyer, 2012 Feldmeyer et al., 2013 Petersen, 2019 Staiger and Petersen, 2021). Elucidation of this circuit organization will be an important step toward characterizing basic mechanisms underlying somatosensory-guided control of the hand and forelimb and related aspects of sensorimotor integration in motor cortex ( Hatsopoulos and Suminski, 2011), and can potentially inform translational approaches to restore hand function in neurological conditions ( Edwards et al., 2019). However, the cellular-level synaptic connectivity linking the major nodes, whereby peripheral inputs are ultimately conveyed to corticospinal neurons in S1 and/or M1, remains largely uncharacterized for these hand-related circuits. The macroscopic structure of these lemnisco-cortical and corticocortical pathways is well-known from classical anatomy ( Brodal, 1981) and supported by in vivo electrophysiology ( Andersson, 1995). The major nodes sequentially traversed in this transcortical pathway include the cuneate nucleus, ventral posterior lateral (VPL) nucleus of thalamus, the hand/forelimb-related primary somatosensory (S1) and motor (M1) cortices. Through a longer loop, somatosensory pathways ascending via brainstem and thalamus reach corticospinal neurons in cortex. At the earliest, most reflexive stage, somatosensory afferents are tightly coupled to motor neurons in the spinal cord. Introductionįunctions of the hand and forelimb depend on sensorimotor circuits spanning multiple levels of the central nervous system ( Kleinfeld et al., 2006 Arber and Costa, 2018). The findings provide a detailed new wiring diagram for the hand/forelimb-related transcortical circuit, delineating a basic but complex set of cell-type-specific feedforward excitatory connections that selectively and extensively engage diverse intratelencephalic projection neurons, thereby polysynaptically linking subcortical somatosensory input to cortical motor output to spinal cord. In the corticocortical leg, S1→M1 connections from L2/3 and L5A neurons mainly excited downstream L2/3 neurons, which excite corticospinal neurons. In the lemnisco-cortical leg, disynaptic cuneate→VPL→S1 connections excited mainly layer (L) 4 neurons. We characterized excitatory connectivity along this pathway in the mouse. For active touch with the hand, the longest loop is the transcortical continuation of ascending pathways, particularly the lemnisco-cortical and corticocortical pathways carrying tactile signals via the cuneate nucleus, ventral posterior lateral (VPL) thalamus, and primary somatosensory (S1) and motor (M1) cortices to reach corticospinal neurons and influence descending activity. Sensory-guided limb control relies on communication across sensorimotor loops.
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