Cortical Reorganization of Sensorimotor Systems and the Role of Intracortical Circuits After Spinal Cord Injury

Abstract

The plasticity of sensorimotor systems in mammals underlies the capacity for motor learning as well as the ability to relearn following injury. Spinal cord injury, which both deprives afferent input and interrupts efferent output, results in a disruption of cortical somatotopy. While changes in corticospinal axons proximal to the lesion are proposed to support the reorganization of cortical motor maps after spinal cord injury, intracortical horizontal connections are also likely to be critical substrates for rehabilitation-mediated recovery. Intrinsic connections have been shown to dictate the reorganization of cortical maps that occurs in response to skilled motor learning as well as after peripheral injury. Cortical networks incorporate changes in motor and sensory circuits at subcortical or spinal levels to induce map remodeling in the neocortex. This review focuses on the reorganization of cortical networks observed after injury and posits a role of intracortical circuits in recovery.

Keywords: Cortical reorganization; Intracortical circuits; Motor cortex; Plasticity; Primates; Rodents; Somatosensory cortex; Spinal cord injury.

Fig. 1

Cortical motor map changes after cervical spinal cord injury in rodents. Representative changes in maps of evoked output in rodents after high (C2–C3) or mid (C4–C5) spinal cord injury. a Topographic organization of the motor cortex in intact rats (adapted from [31]). b High cervical injury results in an aberrant motor map at chronic time points. Intact whisker representations expand into de-efferented areas (adapted from [68]). c Topographic representation of proximal and distal forelimb muscles in CFA and RFA. d After mid-cervical injury and rehabilitation, proximal elbow and shoulder movements expand in both CFA and RFA (adapted from [67])

Fig. 2

Sprouting in brainstem nuclei mediates cortical reorganization after spinal cord injury in primates. a Mechanoreceptive sensory information from the hand and face ascend through the brainstem and thalamic nuclei into area 3b of the somatosensory cortex through parallel pathways. b After cervical spinal cord injury, sprouting occurs within the brainstem as collaterals sprout from trigeminal to cuneate nuclei. This adaptation results in face responses within the de-afferented hand representations in area 3b (adapted from [112, 114])

Fig. 3

Intracortical circuits in area 3b of the somatosensory cortex change after spinal cord injury in primates. a Intracortical connections within the hand and face representations in area 3b of the primate somatosensory cortex span the respective representations but do not cross the hand-face border (adapted from [118]). b After cervical spinal cord injury, face representations expand into parts of the hand representation while sparse, new intracortical connections arise from hand and face regions of area 3b and cross between the two regions (adapted from [119])

Fig. 4

Cortical inputs to forelimb motor areas RFA and CFA in rats. A representative flattened cortical hemisphere with the somatosensory isomorph (black outline) illustrates the patterns of cortical inputs to rostral and caudal forelimb areas (RFA and CFA). A color-coded topographical motor map of evoked movements is shown medially, while primary somatosensory areas are outlined in more caudal and lateral positions. Red and blue markers correspond to individual neurons retrogradely labeled by tracer injection into RFA or CFA, respectively. Injection sites are indicated by dashed outlines (adapted from [10])

Fig. 5

Latent intracortical circuits underlie motor map changes after facial nerve transection in rats. a Intracortical projections arising from the medial part of the whisker representation are restricted to the whisker representation. b Whereas, intracortical projections of the lateral part are more widespread and cross the whisker-forelimb border into the forelimb representation (adapted from [6]). c After facial nerve transection, latent intracortical connections from the lateral whisker area support the medial shift of evoked forelimb motor maps. More medial whisker cortex becomes unresponsive as intrinsic connections are restricted to whisker regions (adapted from [5])