Step training-dependent plasticity in spinal cutaneous pathways

Abstract

Plasticity after spinal cord injury can be initiated by specific patterns of sensory feedback, leading to a reorganization of spinal networks. For example, proprioceptive feedback from limb loading during the stance phase is crucial for the recovery of stepping in spinal-injured animals and humans. Our recent results showed that step training modified transmission from group I afferents of extensors in spinal cats. However, cutaneous afferents are also activated during locomotion and are necessary for proper foot placement in spinal cats. We therefore hypothesized that step training would also modify transmission in cutaneous pathways to facilitate recovery of stepping. We tested transmission in cutaneous pathways by comparing intracellular responses in lumbar motoneurons (n = 136) in trained (n = 11) and untrained (n = 7) cats spinalized 3-5 weeks before the acute electrophysiological experiment. Three cutaneous nerves were stimulated, and each evoked up to three motoneuronal responses mediated by at least three different pathways. Overall, of 71 cutaneous pathways tested, 10 were modified by step training: transmission was reduced in 7 and facilitated in 3. Remarkably, 6 of 10 involved the medial plantar nerve innervating the plantar surface of the foot, including two of the facilitated pathways. Because the cutaneous reflexes are exaggerated after spinalization, we interpret the decrease in most pathways as a normalization of cutaneous transmission necessary to recover locomotor movements. Overall, the results showed a high degree of specificity in plasticity among cutaneous pathways and indicate that transmission of skin inputs signaling ground contact, in particular, is modified by step training.

Figure 2.

Type of responses to cutaneous stimulation recorded in motoneurons. Representative averaged PSP patterns (n ≥ 62) evoked by cutaneous afferents (CCS, MPL, or SP) recorded in extensor or flexor/bifunctional motoneurons are shown. The initial depolarization is referred to as R1, the subsequent hyperpolarization referred to as R2, and the following depolarization referred to as R3. a, Type A response: R1-R2-R3; b, type B response: R2-R3; c, type C response: R2; d, type D response: R1-R3; e, type E response: R1-R2; f, type F response: R1. Baseline is represented by a dotted line from which amplitude is measured for each component (upward and downward arrows). Calibration pulse, 1 mV.

Figure 1.

Training did not modify AHP duration and membrane potential. The histograms of AHP duration (a) and membrane potential (b) of motoneurons in shams (gray) and trained cats (black) show a similar distribution.

Figure 3.

Training specifically modified transmission from cutaneous afferents to the MG motor pool. Left, PSPs (n ≥ 40) evoked by stimulation of CCS (a), MPL (b), and SP (c) afferents recorded in MG motoneurons with similar AHPs (range, 70-91 msec) in a sham (gray) and a trained cat (black). Right, Histograms of the mean amplitude of responses evoked by CCS (a), MPL (b), and SP (c) afferents recorded in all MG motoneurons in shams (gray) and trained cats (black). Six of the nine pathways tested in MG motoneurons were modified by training. Significant differences are indicated as follows: ^*p < 0.05; ^**p < 0.01. Overall, training decreased both CCS-MG-R1 (by 47%) and CCS-MG-R3 (by 61%) (a) amplitude, increased MPL-MG-R1 amplitude (by 89%), decreased MPL-MG-R2 (by 54%) and MPL-MG-R3 (by 46%) (b) amplitude, and decreased SP-MG-R2 amplitude (by 67%) (c). Mn, Motoneuron.

Figure 4.

Training did not modify the phase dependency of cutaneous responses. a, b, PSPs recorded in MG motoneurons evoked by CCS stimuli during the depolarized (gray traces) and hyperpolarized (black traces) phases of the fictive step cycle in the sham (a) and the trained cat (b). The amplitude of the IPSP was decreased in the sham (by 50%) and in the trained cat (by 92%) during the hyperpolarized phase. c, IPSP amplitude was plotted against the LDP for all tested motoneurons in shams (gray) and trained cats (black). No linear relationship was observed between the two values neither in shams (r = 0.41) nor trained cats (r = 0.48). Mn, Motoneuron.

Figure 5.

Clonidine specifically modified transmission from cutaneous afferents to extensor motor pools. Left, PSPs evoked in the same motoneuron before (gray) and after (black) clonidine injection by the stimulation of SP (b, c), MPL (a, e), and CCS (d) in FHL (a, b) and MG (c-e) motoneurons of shams (a) and trained cats (b-e). Right, Histograms of the mean amplitude of responses recorded in all motoneurons in shams (gray) and trained cats (black). Significant differences are indicated as follows: ^*p < 0.05; ^**p < 0.01. Overall, clonidine increased MPL-FHL-R1 (by 258%) and decreased MPL-FHL-R2 (by 100%) amplitude in shams (a), decreased SP-FHL-R2 amplitude in trained cats (by 77%) (b), decreased SP-MG-R2 amplitude in trained cats (by 100%) (c), did not modify amplitude in CCS-MG pathways in trained cats (d), and did not modify amplitude in MPL-MG pathways in trained cats (e). Mn, Motoneuron.