Dual Cortical Plasticity After Spinal Cord Injury

Abstract

During cortical development, plasticity reflects the dynamic equilibrium between increasing and decreasing functional connectivity subserved by synaptic sprouting and pruning. After adult cortical deafferentation, plasticity seems to be dominated by increased functional connectivity, leading to the classical expansive reorganization from the intact to the deafferented cortex. In contrast, here we show a striking "decrease" in the fast cortical responses to high-intensity forepaw stimulation 1-3 months after complete thoracic spinal cord transection, as evident in both local field potentials and intracellular in vivo recordings. Importantly, this decrease in fast cortical responses co-exists with an "increase" in cortical activation over slower post-stimulus timescales, as measured by an increased forepaw-to-hindpaw propagation of stimulus-triggered cortical up-states, as well as by the enhanced slow sustained depolarization evoked by high-frequency forepaw stimuli in the deafferented hindpaw cortex. This coincidence of diminished fast cortical responses and enhanced slow cortical activation offers a dual perspective of adult cortical plasticity after spinal cord injury.

Cortex-dependent recovery of unassisted hindlimb locomotion after complete spinal cord injury in adult rats

“…This overlap of sensorimotor reorganization unifies previous studies on somatosensory (Endo et al, 2007; Kao et al, 2009; Ghosh et al, 2010; Ganzer et al, 2013; Graziano et al, 2013; Humanes-Valera et al, 2017) or motor (Fouad et al, 2001; Giszter et al, 2008; van den Brand et al, 2012; Oza and Giszter, 2014, 2015; Ganzer et al, 2016) reorganization into a joint framework, and is likely to be a key factor for the observed functional recovery. Indeed, lesioning the reorganized cortex reversed the recovery of hindlimb function, without affecting forelimb function.…”

Somatosensory corticospinal tract axons sprout within the cervical cord following a dorsal root/dorsal column spinal injury in the rat

“…No differences, however, were found between the 6-7 and 10-11 week post-lesion periods, which means that the terminal growth had largely occurred within the preceding weeks. If consolidation of these projections over time does occur and if it involves pruning of the exuberance to something approaching pre-lesion ranges (Lorenzana et al, 2015;Humanes-Valera et al, 2017;Nakanishi et al, 2019), this was not evident at 11 post-lesion weeks.…”

Somatosensory corticospinal tract axons sprout within the cervical cord following a dorsal root/dorsal column spinal injury in the rat

“…Given our restricted sample size, it could also be that we had inadequate power to detect any existing difference between post‐lesion periods. If consolidation of these projections over time does occur and if it involves pruning of the exuberance to something approaching pre‐lesion ranges (Humanes‐Valera, Foffani, Alonso‐Calviño, Fernández‐López, & Aguilar, ; Lorenzana, Lee, Mui, Chang, & Zheng, ; Nakanishi, Fujita, & Yamashita, ), this was not evident at 11 post‐lesion weeks.…”