Circuit organization of the excitatory sensorimotor loop through hand/forelimb S1 and M1

Abstract

Sensory-guided limb control relies on communication across sensorimotor loops. 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. We characterized excitatory connectivity along this pathway in the mouse. In the lemnisco-cortical leg, disynaptic cuneate→VPL→S1 connections excited mainly layer (L) 4 neurons. In the corticocortical leg, S1→M1 connections from L2/3 and L5A neurons mainly excited downstream L2/3 neurons, which excite corticospinal neurons. 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.

Manipulation-specific activity in motor and somatosensory cortex as mice handle food

“…Because oromanual movements also involve forelimb somatosensation, we also recorded from the forelimb region of the primary somatosensory (S1) area, located laterally adjacent to forelimb M1 (Yamawaki et al, 2021). Forelimb S1 activity was overall higher during oromanual events compared to holding intervals (mean ± s.d.…”

“…Target coordinates for the three regions were as follows. Forelimb M1: 0.0 mm anterior-posterior (AP), 1.5 mm medial-lateral (ML) (Yamawaki et al, 2021); tongue/jaw M1: 1.8 AP, 2.5 ML (Mayrhofer et al, 2019); forelimb S1: 0.0 mm AP, 2.4 ML. For lateral recording sites (forelimb S1 and tongue/jaw M1), the probes were tilted by ~30° off the vertical axis for alignment with the radial axis of the cortex.…”

Lesion Area in the Cerebral Cortex Determines the Patterns of Axon Rewiring of Motor and Sensory Corticospinal Tracts After Stroke

“…The motor CST functions to gain motor outputs, whereas the sensory CST engages in sensory transmission ( Liu et al, 2018 ; Ueno et al, 2018 ). Furthermore, CFA and S1 have different cortical and subcortical networks ( Edwards et al, 2019 ; Yamawaki et al, 2021 ). The difference in basic connectivity and neural activity may make it difficult to compensate for each pathway and function.…”

Sensory Circuit Remodeling and Movement Recovery After Spinal Cord Injury

“…In rodents, S1 is adjacent to M1 and is the primary source of corticocortical input to forelimb M1, indicating a major role for afferent feedback in shaping motor output ( Colechio and Alloway, 2009 ). Within S1, layer 4, and to a lesser extent layers 2/3 and 5A, receive lemnisco-cortical input from VPL ( Yamawaki et al, 2021 ). Sensory information spreads both vertically and horizontally throughout layer 2/3, suggesting that layer 2/3 S1 circuits integrate information from across diverse brain regions ( Feldmeyer et al, 2013 ).…”

“…Sensory information spreads both vertically and horizontally throughout layer 2/3, suggesting that layer 2/3 S1 circuits integrate information from across diverse brain regions ( Feldmeyer et al, 2013 ). Electrophysiology recordings in response to optogenetic activation in cortical slices have shown that layer 2/3 and 5A S1 corticocortical neurons excite layer 2/3 neurons in M1, with weaker connections to deeper layers ( Yamawaki et al, 2021 ). Within M1, motor learning drives remodeling of both structure and activity of layer 2/3.…”