Abstract
The aim of this study was to investigate the effects of self-reinnervation of the medial (MG) and lateral gastrocnemius (LG) muscles on joint kinematics of the whole hindlimb during overground walking on surfaces of varying slope in the cat. Hindlimb kinematics were assessed (1) with little or no activity in MG and LG (short-term effects of self-reinnervation), and (2) after motor function of these muscles was presumably recovered but their proprioceptive feedback permanently disrupted (long-term effects of self-reinnervation). The stance phase was examined in three walking conditions: downslope (−50%, i.e. −26.6°), level (0%) and upslope (+50%, +26.6°). Measurements were performed prior to and at consecutive time points (between 1 and 57 weeks) after transecting and immediately suturing MG and LG nerves. It was found that MG-LG self-reinnervation did not significantly change hip height and hindlimb orientation in any of the three walking conditions. Substantial short-term effects were observed in the ankle joint (e.g., increased flexion in early stance) as well as in metatarsophalangeal and knee joints, leading to altered interjoint coordination. Hindlimb kinematics in level and upslope walking progressed back towards baseline within 14–19 weeks. Thus in these two conditions the cats were walking without any detectable kinematic deficits, despite the absence of length feedback from two major ankle extensors. This was verified in a decerebrate preparation for four of the five cats. In contrast, ankle joint kinematics as well as interjoint coordination in downslope walking gradually progressed towards, but never reached their baseline patterns. The short-term effects can be explained by both mechanical and neural factors that are affected by the functional elimination of MG and LG. Permanent changes in kinematics during downslope walking indicate the importance of proprioceptive feedback from the MG and LG muscles in regulating locomotor activity of ankle extensors. Full recovery of hindlimb kinematics during level and upslope walking suggests that the proprioceptive loss is compensated by other sensory sources (e.g. cutaneous receptors) or altered central drive.
Similar content being viewed by others
References
Abelew TA, Miller MD, Cope TC, Nichols TR (2000) Local loss of proprioception results in disruption of interjoint coordination during locomotion in the cat. J Neurophysiol 84:2709–2714
Bouyer LJG, Whelan PJ, Pearson KG, Rossignol S (2001) Adaptive locomotor plasticity in chronic spinal cats after ankle extensors neurectomy. J Neurosci 21:3531–3541
Burkholder TJ, Nichols TR (2004) Three-dimensional model of the feline hindlimb. J Morphol 261:118–129
Carlson-Kuhta P, Trank TV, Smith JL (1998) Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking. J Neurophysiol 79:1687–1701
Carrier L, Brustein E, Rossignol S (1997) Locomotion of the hindlimbs after neurectomy of ankle flexors in intact and spinal cats: model for the study of locomotor plasticity. J Neurophysiol 77:1979–1993
Cope TC, Bonasera SJ, Nichols TR (1994) Reinnervated muscles fail to produce stretch reflexes. J Neurophysiol 71:817–820
Cope TC, Clark BD (1993) Motor-unit recruitment in self-reinnervated muscle. J Neurophysiol 70:1787–1796
Cope TC, Webb CB, Botterman BR (1991) Control of motor-unit tension by rate modulation during sustained contractions in reinnervated cat muscle. J Neurophysiol 65:648–656
Davis LA, Gordon T, Hoffer JA, Jhamandas J, Stein RB (1978) Compound action potentials recorded from mammalian peripheral nerves following ligation or resuturing. J Physiol 285:543–559
Engberg I, Lundberg A (1969) An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. Acta Physiol Scand 75:614–630
English AW (1984) An electromyographic analysis of compartments in cat lateral gastrocnemius muscle during unrestrained locomotion. J Neurophysiol 52:114–125
Foehring RC, Sypert GW, Munson JB (1986) Properties of self-reinnervated motor units of medial gastrocnemius of cat. II. Axotomized motoneurons and time course of recovery. J Neurophysiol 55:947–965
Fowler EG, Gregor RJ, Hodgson JA, Roy RR (1993) Relationship between ankle muscle and joint kinetics during the stance phase of locomotion in the cat. J Biomech 26:465–483
Fowler EG, Gregor RJ, Roy RR (1988) Differential kinetics of fast and slow ankle extensors during the paw-shake in the cat. Exp Neurol 99:219–224
Gordon T, Stein RB (1982a) Reorganization of motor-unit properties in reinnervated muscles of the cat. J Neurophysiol 48:1175–1190
Gordon T, Stein RB (1982b) Time course and extent of recovery in re-innervated motor units of cat triceps surae muscles. J Physiol Lond 323:307–323
Goslow GE Jr, Reinking RM, Stuart DG (1973) The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141:1–41
Gregor RJ, Prilutsky BI, Nichols TR, Smith DW (2003) EMG output in reinnervated medial gastrocnemius muscle during locomotion in the cat. Program No. 493.8. Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington
Gregor RJ, Smith DW, Prilutsky BI (2006) Mechanics of slope walking in the cat: quantification of muscle load, length change and ankle extensor EMG patterns. J Neurophysiol 95:1397–1409
Gregor RJ, Smith JL, Smith DW, Oliver A, Prilutsky BI (2001) Hindlimb kinetics and neural control during slope walking in the cat: unexpected findings. J Appl Biomech 17:277–286
Haftel VK, Bichler EK, Wang QB, Prather JF, Pinter MJ, Cope TC (2005) Central suppression of regenerated proprioceptive afferents. J Neurosci 25:4733–4742
Herzog W, Leonard TR, Guimaraes AC (1993) Forces in gastrocnemius, soleus, and plantaris tendons of the freely moving cat. J Biomech 26:945–953
Huyghues-Despointes CM, Cope TC, Nichols TR (2003a) Intrinsic properties and reflex compensation in reinnervated triceps surae muscles of the cat: effect of activation level. J Neurophysiol 90:1537–1546
Huyghues-Despointes CM, Cope TC, Nichols TR (2003b) Intrinsic properties and reflex compensation in reinnervated triceps surae muscles of the cat: effect of movement history. J Neurophysiol 90:1547–1555
Kaya M, Leonard T, Herzog W (2003) Coordination of medial gastrocnemius and soleus forces during cat locomotion. J Exp Biol 206:3645–3655
Lehmann JF, Condon SM, Delateur BJ, Smith JC (1985) Gait Abnormalities in Tibial Nerve Paralysis - a Biomechanical Study. Arch Phys Med Rehabil 66:80–85
Lin FM, Pan YC, Dinh TA, Sabbahi M, Shenaq S (1997) Functional assessment of tibial-nerve recovery in the cat using gait analysis: preliminary study. J Reconstr Microsurg 13:177–183
Maas H, Prilutsky BI, Gregor RJ (2005) In vivo fascicle length of cat medial gastrocnemius and soleus muscles during slope walking. In: XXth congress of the international society of biomechanics. Cleveland, p 90
Maas H, Prilutsky BI, Welch T, Gregor RJ (2004) Reinnervation of the gastrocnemius muscle in the cat: immediate and long-term effects in interjoint coordination. Program No. 180.6. Abstract viewer/itinerary planner. Society for Neuroscience, Washington
Misiaszek JE, Pearson KG (2002) Adaptive changes in locomotor activity following botulinum toxin injection in ankle extensor muscles of cats. J Neurophysiol 87:229–239
Nichols TR (1989) The organization of heterogenic reflexes among muscles crossing the ankle joint in the decerebrate cat. J Physiol 410:463–477
Nichols TR (1994) A biomechanical perspective on spinal mechanisms of coordinated muscular action: an architecture principle. Acta Anat 151:1–13
Nichols TR (1999) Receptor mechanisms underlying heterogenic reflexes among the triceps surae muscles of the cat. J Neurophysiol 81:467–478
Nichols TR, Houk JC (1976) Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. J Neurophysiol 39:119–142
Pearson KG, Fouad K, Misiaszek JE (1999) Adaptive changes in motor activity associated with functional recovery following muscle denervation in walking cats. J Neurophysiol 82:370–381
Prilutsky BI, Gregor RJ, Nichols TR (2004) Coordination of cat ankle extensors during the paw-shake before and after self-reinnervation of medial and lateral gastrocnemius muscles. Program No. 69.12. Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington
Prilutsky BI, Herzog W, Allinger TL (1994) Force-sharing between cat soleus and gastrocnemius muscles during walking: explanations based on electrical activity, properties, and kinematics. J Biomech 27:1223–1235
Prilutsky BI, Herzog W, Leonard T (1996) Transfer of mechanical energy between ankle and knee joints by gastrocnemius and plantaris muscles during cat locomotion. J Biomech 29:391–403
Prilutsky BI, Maas H, Gregor RJ (2005a) In vivo fascicle velocity of cat gastrocnemius and soleus muscles during the paw-shake. In: XXth Congress of the International Society of Biomechanics, Cleveland
Prilutsky BI, Maas H, Gregor RJ (2006a) Ankle joint moment during walking after self-reinntervation of selected ankle extensors in the cat. In: American Society of Biomechanics, Blacksburg, Virginia
Prilutsky BI, Maas H, Nichols TR, Gregor RJ (2006b) Effects of self-reinnervation of selected cat ankle extensors on their activity and hindlimb mechanics in slope walking. Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington
Prilutsky BI, Sirota MG, Gregor RJ, Beloozerova IN (2005b) Quantification of motor cortex activity and full-body biomechanics during unconstrained locomotion. J Neurophysiol 94:2959–2969
Ross KT, Huyghues-Despointes CMJ, Nichols TR (2003) Heterogenic feedback among quadriceps and ankle extensors during spontaneous locomotion in premammillary cats. Program No. 276.11. Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington
Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389–442
Simon SR, Mann RA, Hagy JL, Larsen LJ (1978) Role of posterior calf muscles in normal gait. J Bone Joint Surg 60:465–472
Smith JL, Betts B, Edgerton VR, Zernicke RF (1980) Rapid ankle extension during paw shakes—selective recruitment of fast ankle extensors. J Neurophysiol 43:612–620
Smith JL, Carlson-Kuhta P, Trank TV (1998) Forms of forward quadrupedal locomotion. III. A comparison of posture, hindlimb kinematics, and motor patterns for downslope and level walking J Neurophysiol 79:1702–1716
Trank TV, Chen C, Smith JL (1996) Forms of forward quadrupedal locomotion. I. A comparison of posture, hindlimb kinematics, and motor patterns for normal and crouched walking J Neurophysiol 76:2316–2326
Trank TV, Smith JL (1996) Adaptive control for backward quadrupedal walking VI. metatarsophalangeal joint dynamics and motor patterns of digit muscles. J Neurophysiol 75:678–679
Walmsley B, Hodgson JA, Burke RE (1978) Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. J Neurophysiol 41:1203–1216
Wetzel MC, Gerlach RL, Stern LZ, Hannapel LK (1973) Behavior and histochemistry of functionally isolated cat ankle extensors. Exp Neurol 39:223–233
Whiting WC, Gregor RJ, Roy RR, Edgerton VR (1984) A technique for estimating mechanical work of individual muscles in the cat during treadmill locomotion. J Biomech 17:685–694
Wilmink RJ, Nichols TR (2003) Distribution of heterogenic reflexes among the quadriceps and triceps surae muscles of the cat hind limb. J Neurophysiol 90:2310–2324
Zhong H, Roy RR, Monti RJ, Edgerton VR (2005) Mechanical responses of the cat plantaris muscle to chronic functional overload: in vivo and in situ measurements. Program No. 397.11. Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington
Acknowledgments
The authors thank Webb Smith for recruiting skilled students and managing the continuously growing data base and Dr. Guayhaur Shue for technical support. In addition, we thank Drs. Clotilde Huyghues-Despointes and Kyla Ross for assisting in terminal experiments to test the integrity of reflex pathways and Dr. Michael Kutner for statistical advice. This research was supported by National Institutes of Health Grants HD032571 and NS048844 as well as the Center for Human Movement Studies at the Georgia Institute of Technology.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Maas, H., Prilutsky, B.I., Nichols, T.R. et al. The effects of self-reinnervation of cat medial and lateral gastrocnemius muscles on hindlimb kinematics in slope walking. Exp Brain Res 181, 377–393 (2007). https://doi.org/10.1007/s00221-007-0938-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-007-0938-8