Non-uniform upregulation of the autogenic stretch reflex among hindlimb extensors following lateral spinal lesion in the cat

Abstract

Successful propagation throughout the step cycle is contingent on adequate regulation of whole-limb stiffness by proprioceptive feedback. Following spinal cord injury (SCI), there are changes in the strength and organization of proprioceptive feedback that can result in altered joint stiffness. In this study, we measured changes in autogenic feedback of five hindlimb extensor muscles following chronic low thoracic lateral hemisection (LSH) in decerebrate cats. We present three features of the autogenic stretch reflex obtained using a mechanographic method. Stiffness was a measure of the resistance to stretch during the length change. The dynamic index documented the extent of adaptation or increase of the force response during the hold phase, and the impulse measured the integral of the response from initiation of a stretch to the return to the initial length. The changes took the form of variable and transient increases in the stiffness of vastus (VASTI) group, soleus (SOL), and flexor hallucis longus (FHL), and either increased (VASTI) or decreased adaptation (GAS and PLANT). The stiffness of the gastrocnemius group (GAS) was also variable over time but remained elevated at the final time point. An unexpected finding was that these effects were observed bilaterally. Potential reasons for this finding and possible sources of increased excitability to this muscle group are discussed.

Keywords: Extensor muscles; Hemisection; Ia pathway; Length feedback.

Fig. 1

Force response and its features. The force response (FR) is force generated by a muscle as it resists a stretch. It can be characterized by (i) stiffness (k), which is change in force over change in length, (ii) peak of the dynamic response (max(D)), and (iii) adaptation to hold (dFs-d) as the muscle is held isometrically. The background force (BGF) was removed prior to the analysis. The early force response is composed of a mechanical component (F_m) prior to ~ 18 ms after the stretch onset. The time point when the slope increases, where the neural component (F_d) begins, is the latency of the stretch reflex.

Fig. 2

Changes in impulse (a), stiffness (b), and dynamic index (c) of VASTI across three recovery time points. Both impulse and stiffness significantly increase after the injury and gradually subside to the control values. Dynamic index decreases, becoming negative between 3 and 7 weeks and significantly different from control values by 13 weeks post-injury. Open circles represent left and contralateral limb in CNT and LSH groups, respectively, whereas filled triangles represent data obtained from the right and ipsilateral limb in CNT and LSH groups. The CNT limbs are presented using different symbols to show across limbs and cats data distribution of CNT. Significance levels: * = p ≤ 0.050, ** = p ≤ 0.010, *** = p ≤ 0.005. All subsequent figures follow the same convention

Fig. 3

Changes in impulse (a), stiffness (b), and dynamic index (c) of GAS across three recovery time points. All features increase 3 weeks after the injury with impulse and stiffness increase reaching significance. The impulse and stiffness show an oscillatory trend where these features transiently return toward the CNT values at 7 weeks but then increase again. The dynamic index was less negative throughout the recovery time points, compared to the CNT group, although it approached CNT values at the last time point. Open circles represent left and contralateral limb in CNT and LSH groups respectively, while filled triangles represent data obtained from the right and ipsilateral limb in CNT and LSH groups

Fig. 4

Changes in impulse (a), stiffness (b), and dynamic index (c) of PLANT across three recovery time points. Neither impulse nor stiffness was significantly affected by the lesion, although the dynamic index increased transiently at the 7 week recovery time point. Open circles represent left and contralateral limb in CNT and LSH groups respectively, while filled triangles represent data obtained from the right and ipsilateral limb in CNT and LSH groups

Fig. 5

Changes in impulse (a), stiffness (b), and dynamic index (c) of SOL across three recovery time points. Both stiffness and impulse of SOL increase following the injury and subsidies to control values with time. The dynamic index shows no change throughout the recovery time periods. Open circles represent left and contralateral limb in CNT and LSH groups respectively, while filled triangles represent data obtained from the right and ipsilateral limb in CNT and LSH groups

Fig. 6

Changes in impulse (a), stiffness (b), and dynamic index (c) of FHL across three recovery time points. Both stiffness and impulse are affected by LSH, while dynamic index does not differ from CNT values. Open circles represent left and contralateral limb in CNT and LSH groups respectively, while filled triangles represent data obtained from the right and ipsilateral limb in CNT and LSH groups