Adaptive locomotor plasticity in chronic spinal cats after ankle extensors neurectomy

Abstract

After lateral gastrocnemius-soleus (LGS) nerve section in intact cats, a rapid locomotor compensation involving synergistic muscles occurs and is accompanied by spinal reflex changes. Only some of these changes are maintained after acute spinalization, indicating the involvement of descending pathways in functional recovery. Here, we address whether the development of these adaptive changes is dependent on descending pathways. The left LGS nerve was cut in three chronic spinal cats. Combined kinematics and electromyographic (EMG) recordings were obtained before and for 8 d after the neurectomy. An increased yield at the ankle was present early after neurectomy and, as in nonspinal cats, was gradually reduced within 8 d. Compensation involved transient changes in step cycle structure and a longer term increase in postcontact medial gastrocnemius (MG) EMG activity. Precontact MG EMG only increased in one of three cats. In a terminal experiment, the influence of group I afferents from MG and LGS on stance duration was measured in two cats. LGS effectiveness at increasing stance duration was largely decreased in both cats. MG effectiveness was only slightly changed: increased in one cat and decreased in another. In cat 3, the plantaris nerve was cut after LGS recovery. The recovery time courses from both neurectomies were similar (p > 0.8), suggesting that this spinal compensation is likely a generalizable adaptive strategy. From a functional perspective, the spinal cord therefore must be considered capable of adaptive locomotor plasticity after motor nerve lesions. This finding is of prime importance to the understanding of functional plasticity after spinal injury.

Fig. 1.

A, C. Stick figure reconstructions of the left hindlimb generated from a frame-by-frame video analysis during locomotion at a treadmill speed of 0.4 m/sec before (A) and 1 d after cutting the left LGS nerve (C) in cat 2. B,D, Top traces, Raw EMG data obtained during the bouts of locomotion from which A andC were taken. Bottom traces, Left and right hindlimb duty cycles. Downward arrows represent foot contact, upward arrows represent foot lift, anddark horizontal lines represent stance phase. This cat was spinalized 24 d before the LGS neurectomy.LMG, Left MG; RMG, right MG.

Fig. 2.

A, Stick figure reconstructions of the left hindlimb before (top), and 2 d (middle) and 8 d (bottom) after the neurectomy. B, Details of the angular excursions during the step cycle obtained before (n = 23; pale gray traces), and 2 d (n = 11;black traces) and 8 d (n = 9;dark gray traces) after the LGS neurectomy for cat 3.C, Time course of ankle angle (±SD) at φ = 0.3 (which represents maximum yield) superimposed for all cats. *p < 0.05.

Fig. 3.

A, Line drawing traced from a video image taken at foot contact for cat 1 in the control situation.B, Average (±SD) horizontal toe position with respect to the hip for the three cats. C, D, Same as A and B, but for foot position at foot lift. *p < 0.05.

Fig. 4.

Double support phases (time at which the two feet are on the ground) at the left to right stance transition (double support 1; A) and right to left stance transition (double support 2; B) as a function of time after the neurectomy. C, D, E, Mean (±SD) timing of right foot lift (C), right foot contact (D), and left foot lift (E) with respect to left foot contact as a function of time after the neurectomy. *p < 0.05.

Fig. 5.

Left, Normalized mean EMG amplitude (±SD) for left and right medial gastrocnemii and left vastus lateralis muscles against time after the lesion.Right, Average EMG burst durations in msec (±SD) for these muscles against time after the lesion. *p < 0.05.

Fig. 6.

A–C, Average rectified EMG envelopes of the MG muscle, early (2 d) and late (8 d) after the neurectomy in dark traces compared with control ± SEM in gray traces. D–F, Time course of changes in precontact (closed circles) and postcontact (open circles) EMG as a function of time after the LGS neurectomy.

Fig. 7.

Normalized mean (MG EMG) amplitude (±SD) and calculated MG muscle length (±SD) at a normalized phase of 0.3 with respect to foot contact. *p < 0.05.

Fig. 8.

A, Mean ankle angles (±SD) after LGS (closed circles) and subsequent PL (open circles) neurectomies in cat 3. Control, Last two walking sessions before each neurectomy.There was no statistical difference between the two curves (p > 0.8). B, Average rectified MG EMG profiles synchronized on foot contact before and 2 and 8 d after the LGS neurectomy. C, Average rectified MG EMG profiles synchronized on foot contact before and 1 and 11 d after the PL neurectomy. The scales are identical in Band C.

Fig. 9.

A, Raw data obtained from the control (right) leg to stimulation of the right LGS nerve at 2 × T. B, Raw data from the neurectomized leg obtained during stimulation of the left LGS nerve at 2 × T.C, Efficiency of LGS nerve stimulation at increasing step cycle duration represented by frequency histograms.D, Same as C, but for MG stimulation. ○, Intact leg; ●, neurectomized leg.