Top

Published in:

Open Access 01-06-2010 | Research Article

Locomotor changes in length and EMG activity of feline medial gastrocnemius muscle following paralysis of two synergists

Authors: Huub Maas, Robert J. Gregor, Emma F. Hodson-Tole, Brad J. Farrell, Arthur W. English, Boris I. Prilutsky

Published in: Experimental Brain Research | Issue 4/2010

Abstract

The mechanism of the compensatory increase in electromyographic activity (EMG) of a cat ankle extensor during walking shortly after paralysis of its synergists is not fully understood. It is possible that due to greater ankle flexion in stance in this situation, muscle spindles are stretched to a greater extent and, thus, contribute to the EMG enhancement. However, also changes in force feedback and central drive may play a role. The aim of the present study was to investigate the short-term (1- to 2-week post-op) effects of lateral gastrocnemius (LG) and soleus (SO) denervation on muscle fascicle and muscle–tendon unit (MTU) length changes, as well as EMG activity of the intact medial gastrocnemius (MG) muscle in stance during overground walking on level (0%), downslope (−50%, presumably enhancing stretch of ankle extensors in stance) and upslope (+50%, enhancing load on ankle extensors) surfaces. Fascicle length was measured directly using sonomicrometry, and MTU length was calculated from joint kinematics. For each slope condition, LG-SO denervation resulted in an increase in MTU stretch and peak stretch velocity of the intact MG in early stance. MG muscle fascicle stretch and peak stretch velocity were also higher than before denervation in downslope walking. Denervation significantly decreased the magnitude of MG fascicle shortening and peak shortening velocity during early stance in level and upslope walking. MG EMG magnitude in the swing and stance phases was substantially greater after denervation, with a relatively greater increase during stance of level and upslope walking. These results suggest that the fascicle length patterns of MG muscle are significantly altered when two of its synergists are in a state of paralysis. Further, the compensatory increase in MG EMG is likely mediated by enhanced MG length feedback during downslope walking, enhanced feedback from load-sensitive receptors during upslope walking and enhanced central drive in all walking conditions.

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 84:2709–2714PubMed

Biewener AA, Corning WR, Tobalske BW (1998a) In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livia). J Exp Biol 201:3293–3307PubMed

Biewener AA, Konieczynski DD, Baudinette RV (1998b) In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies. J Exp Biol 201:1681–1694PubMed

Bouyer LJG, Whelan PJ, Pearson KG, Rossignol S (2001) Adaptive locomotor plasticity in chronic spinal cats after ankle extensors neurectomy. J Neurosci 21:3531–3541PubMed

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 77:1979–1993PubMed

Conway BA, Hultborn H, Kiehn O (1987) Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res 68:643–656CrossRefPubMed

Cope TC, Webb CB, Botterman BR (1991) Control of motor-unit tension by rate modulation during sustained contractions in reinnervated cat muscle. J Neurophysiol 65:648–656PubMed

Cope TC, Bonasera SJ, Nichols TR (1994) Reinnervated muscles fail to produce stretch reflexes. J Neurophysiol 71:817–820PubMed

Donelan JM, Pearson KG (2004) Contribution of force feedback to ankle extensor activity in decerebrate walking cats. J Neurophysiol 92:2093–2104CrossRefPubMed

Donelan JM, Mcvea DA, Pearson KG (2009) Force regulation of ankle extensor muscle activity in freely walking cats. J Neurophysiol 101:360–371CrossRefPubMed

English AW (1984) An electromyographic analysis of compartments in cat lateral gastrocnemius muscle during unrestrained locomotion. J Neurophysiol 52:114–125PubMed

English AW, Letbetter WD (1982) Anatomy and innervation patterns of cat lateral gastrocnemius and plantaris muscle. Am J Anat 164:66–77CrossRef

English AW, Meador W, Carrasco DI (2005) Neurotrophin-4/5 is required for the early growth of regenerating axons in peripheral nerves. Eur J Neurosci 21:2624–2634CrossRefPubMed

Frigon A, Rossignol S (2007) Plasticity of reflexes from the foot during locomotion after denervating ankle extensors in intact cats. J Neurophysiol 98:2122–2132CrossRefPubMed

Gorassini MA, Prochazka A, Hiebert GW, Gauthier MJ (1994) Corrective responses to loss of ground support during walking. I. Intact cats. J Neurophysiol 71:603–610PubMed

Gordon T, Stein RB (1982) Time course and extent of recovery in re-innervated motor units of cat triceps surae muscles. J Physiol-Lond 323:307–323PubMed

Goslow GE Jr, Reinking RM, Stuart DG (1973) The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141:1–41CrossRefPubMed

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

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 95:1397–1409CrossRefPubMed

Griffiths RI (1991) Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance. J Physiol 436:219–236PubMed

Gritsenko V, Mushahwar V, Prochazka A (2001) Adaptive changes in locomotor control after partial denervation of triceps surae muscles in the cat. J Physiol-Lond 533:299–311CrossRefPubMed

Guertin P, Angel MJ, Perreault MC, Mccrea DA (1995) Ankle extensor group-I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. J Physiol-Lond 487:197–209PubMed

Hiebert GW, Pearson KG (1999) Contribution of sensory feedback to the generation of extensor activity during walking in the decerebrate cat. J Neurophysiol 81:758–770PubMed

Hoffer JA, Caputi AA, Pose IE, Griffiths RI (1989) Roles of muscle activity and load on the relationship between muscle spindle length and whole muscle length in the freely walking cat. Progress in Brain Research 80: 75–85; discussion 57–60

Maas H, Lichtwark GA (2009) Is muscle-tendon unit length a valid indicator for muscle spindle output? J Physiology (Lond) 587:13–14CrossRef

Maas H, Prilutsky BI, Nichols TR, Gregor RJ (2007) The effects of self-reinnervation of cat medial and lateral gastrocnemius muscles on hindlimb kinematics in slope walking. Exp Brain Res 181:377–393CrossRefPubMed

Maas H, Gregor RJ, Hodson-Tole EF, Farrell BJ, Prilutsky BI (2009) Distinct muscle fascicle length changes in feline medial gastrocnemius and soleus muscles during slope walking. J Appl Physiol 106:1169–1180CrossRefPubMed

Misiaszek JE, Pearson KG (2002) Adaptive changes in locomotor activity following botulinum toxin injection in ankle extensor muscles of cats. J Neurophysiol 87:229–239PubMed

Nichols TR, Houk JC (1976) Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. J Neurophysiol 39:119–142PubMed

Pearson KG, Collins DF (1993) Reversal of the influence of group Ib afferents from plantaris on activity in medial gastrocnemius-muscle during locomotor-activity. J Neurophysiol 70:1009–1017PubMed

Pearson KG, Misiaszek JE (2000) Use-dependent gain change in the reflex contribution to extensor activity in walking cats. Brain Res 883:131–134CrossRefPubMed

Pearson KG, Misiaszek JE, Fouad K (1998) Enhancement and resetting of locomotor activity by muscle afferents. Ann N Y Acad Sci 860:203–215CrossRefPubMed

Pearson KG, Fouad K, Misiaszek JE (1999) Adaptive changes in motor activity associated with functional recovery following muscle denervation in walking cats. J Neurophysiol 82:370–381PubMed

Phillipson M (1905) L’autonomie et la centralization dans le systeme nerveux des animaux. Travails du Laboratoire de la Physiologie, Institut Solvey 7:1–208

Pratt CA, Chanaud CM, Loeb GE (1991) Functionally complex muscles of the cat hindlimb.4. Intramuscular distribution of movement command signals and cutaneous reflexes in broad, bifunctional thigh muscles. Exp Brain Res 85:281–299CrossRefPubMed

Prilutsky BI, Herzog W, Leonard TR, Allinger TL (1996) Role of the muscle belly and tendon of soleus, gastrocnemius, and plantaris in mechanical energy absorption and generation during cat locomotion. J Biomech 29:417–434CrossRefPubMed

Prilutsky BI, Sirota MG, Gregor RJ, Beloozerova IN (2005) Quantification of motor cortex activity and full-body biomechanics during unconstrained locomotion. J Neurophysiol 94:2959–2969CrossRefPubMed

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

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. In: Society for Neuroscience, Atlanta

Prochazka A (1999) Quantifying proprioception. Prog Brain Res 123:133–142CrossRefPubMed

Ross KT, Nichols TR (2009) Heterogenic feedback between hindlimb extensors in the spontaneously locomoting premammillary cat. J Neurophysiol 101:184–197CrossRefPubMed

Rossignol S, Dubuc RJ, Gossard JP (2006) Dynamic sensorimotor interactions in locomotion. Physiol Rev 86:89–154CrossRefPubMed

Whelan PJ, Pearson KG (1997) Comparison of the effects of stimulating extensor group I afferents on cycle period during walking in conscious and decerebrate cats. Exp Brain Res 117:444–452CrossRefPubMed

Windhorst U (2008) Muscle spindles are multi-functional. Brain Res Bull 75:507–508CrossRefPubMed

Title: Locomotor changes in length and EMG activity of feline medial gastrocnemius muscle following paralysis of two synergists
Authors: Huub Maas
Robert J. Gregor
Emma F. Hodson-Tole
Brad J. Farrell
Arthur W. English
Boris I. Prilutsky
Publication date: 01-06-2010
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 4/2010
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-010-2279-2

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Locomotor changes in length and EMG activity of feline medial gastrocnemius muscle following paralysis of two synergists

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2010

A diverse pattern of the spike threshold changes in feline gastrocnemius–soleus motoneurons during stretch reflex activation

Adaptation of within-object saccades can be induced by changing stimulus size

To me or to you? When the self is advantaged

Attentional influences on the performance of secondary physical tasks during posture control

Antisaccades exhibit diminished online control relative to prosaccades

Recovery of function following unilateral damage to visuoparietal cortex