Abstract
During stereotyped behaviors such as locomotion, patterns of muscle recruitment are usually quite consistent from animal to animal, even in the face of many surgical and pharmacological reductions. However, as studies of musculoskeletal structure, neuromuscular architecture, and sensorimotor circuitry become more detailed, it is important to ask whether there is some level of organization at which individual differences begin to dominate. This study concentrated on the small muscles of the foot and ankle, using standardized methods that consistently record stereotypical electromyographic activity from prime mover muscles and that permit wellcalibrated stimulation of cutaneous nerves to elicit reflexes during treadmill locomotion. Some muscles (particularly the main ankle extensors, triceps surae, and plantaris) had stereotyped activity during both unperturbed locomotion and reflex responses. Others had stereotyped activity during locomotion but variable reflex patterns among animals (tibialis anterior, extensor digitorum longus, flexor hallucis longus, and peroneus brevis). Still others had variable locomotor activity but reflexes that were consistent (flexor digitorum longus) or variable for only peroneal nerve stimulation (peroneus longus), only plantar nerve stimulation (peroneus tertius), or the two (flexor digitorum brevis). Among muscles with interanimal variability, there seemed to be no particular correlation between locomotor and reflexive recruitment in a given animal. This functional heterogeneity is discussed in terms of the development of locomotor and reflex programs and in the context of structural heterogeneity of some of these muscles that is described in the companion paper.
Similar content being viewed by others
References
Abraham LD, Loeb GE (1985) The distal hindlimb musculature of the cat. Patterns of normal use. Exp Brain Res 58:580–593
Abraham LD, Marks WB, Loeb GE (1985) The distal hindlimb musculature of the cat. Cutaneous reflexes during locomotion. Exp Brain Res 58:594–603
Bak MJ, Loeb GE (1979) A pulsed integrator for EMG analysis. Electroencephalogr Clin Neurophysiol 47:738–741
Blaszczyk JW, Loeb GE (1993) Why cats pace on the treadmill. Physiol Behav 53:501–507
Burgess PR, Petit D, Warren RM (1968) Receptor types in cat hairy skin supplied by myelinated fibers. J Neurophysiol 31:833–848
Burke RE, Fleshman JW (1986) Strategies to identify interneurons involved in locomotor pattern generation in the mammalian spinal cord. In: Grillner S, Stein PSG, Stuart DG (eds) Neurobiology of vertebrate locomotion. Macmillan, London, pp 245–268
Cavanagh PR, Lafortune M (1980) Ground reaction forces in distance running. J Biomech 13:397–406
Chanaud CM, Pratt CA, Loeb GE (1991) Functionally complex muscles of the cat hindlimb. V. The roles of histochemical fibertype regionalization and mechanical heterogeneity in differenttial muscle activation. Exp Brain Res 85:300–313
Chow CK, Jacobson DH (1971) Studies of human locomotion via optimal programming. Math Biosci 10:239–306
Cole KJ, Abbs JH (1987) Kinematic and electromyographic responses to perturbation of a rapid grasp. J Neurophysiol 57:1498–1510
Coss L, Chan AK, Goslow GE, Rasmussen S (1978) Ipsilateral limb variation in cats during overground locomotion. Brain Behav Evol 15:85–93
Davy DT, Audu ML (1987) A dynamic optimization technique for predicting muscle forces in the swing phase of gait. J Biomech 20:187–201
Delcomyn F (1980) Neural basis of rhythmic behavior in animals. Science 210:492–498
Duenas SH, Loeb GE, Marks WB (1984) A quantitative comparison of hindlimb muscle activity and flexor reflexes in normal and decerebrate cats during walking. Soc Neurosci Abstr 10:628
Duysens J, Loeb GE (1980) Modulation of ipsi- and contralateral reflex responses in unrestrained walking cats. J Neurophysiol 44:1024–1037
Duysens J, Stein RB (1978) Reflexes induced by nerve stimulation in walking cats with implanted electrodes. Exp Brain Res 32:213–224
Eccles RM, Lundberg A (1959a) Supraspinal control of interneurones mediating spinal reflexes. J Physiol (Lond) 147:565–584
Eccles RM, Lundberg A (1959b) Synaptic actions in motoneurons by afferents which may evoke the flexion reflex. Arch Ital Biol 97:199–221
Engberg I (1964) Reflexes to foot muscles in the cat. Acta Physiol Scand 62 (Suppl 235):46–64
Fleshman JW, Lev-Tov A, Burke RE (1984) Peripheral and central control of flexor digitorum longus and flexor hallicus longus motoneurons: the synaptic basis of functional diversity. Exp Brain Res 54:133–149
Fleshman JW, Rudomin P, Burke RE (1988) Supraspinal control of a short-latency cutaneous pathway to hindlimb motoneurons. Exp Brain Res 69:449–459
Forssberg H, Svartengren G (1983) Hardwired locomotor network in cat revealed by a retained motor pattern to gastrocnemius after muscle transposition. Neurosci Lett 41:283–288
Forssberg H, Grillner S, Rossignol S (1975) Phase dependent reflex reversal during walking in chronic spinal cats. Brain Res 85:103–107
Forssberg H, Grillner S, Rossignol S (1977) Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion. Brain Res 132:121–139
Gracco VL, Abbs JH (1985) Dynamic control of the perioral system during speech: kinematic analyses of autogenic and nonautogenic sensorimotor processes. J Neurophysiol 54:418–432
Graham Brown T (1911) The intrinsic factors in the act of progression in the mammal. Proc R Soc Lond [Biol] 84:308–319
Grillner S, Zangger P (1975) How detailed is the central pattern generation for locomotion? Brain Res 88:367–371
Halbertsma J (1983) The stride cycle of the cat: the modeling of locomotion by computerized analysis of automatic recordings. Acta Physiol Scand [Suppl] 521:1–75
Hoffer JA, Loeb GE, Pratt CA (1981) Unitary axonal conduction velocity from averaged nerve cuff electrodes in cats. J Neurosci Methods 4:211–225
Hoffer JA, Loeb GE, Marks WB, O'Donovan MJ, Pratt CA, Sugano N (1987) Cat hindlimb motoneurons during locomotion. I. Destination, axonal conduction velocity and recruitment threshold. J Neurophysiol 57:510–529
Hogan N (1984) Adaptive control of mechanical impedance by coactivation of antagonist muscles. IEEE Trans Autom Control 29:681–690
Kanda K, Burke RE, Walmsley B (1977) Differential control of fast and slow twitch motor units in the decerebrate cat. Exp Brain Res 29:57–74
Kernell D, Hultborn H (1990) Synaptic effects on recruitment gain: a mechanism of importance for the input-output relations of motoneurone pools? Brain Res 507:176–170
LaBella LA, Kehler JP, McCrea DA (1989) A differential synaptic input to the motor nuclei of triceps surae from the caudal and lateral cutaneous sural nerves. J Neurophysiol 61:291–301
Leffert RP (1976) Patterns of neuromuscular activity following tendon transfer in the upper limb: a preliminary study. J Hand Surg 1:181–189
Lockard DL, Traher LM, Wetzel MC (1976) Reinforcement influences upon topography of treadmill locomotion by cats. Physiol Behav 16:141–146
Loeb GE (1987) Cutaneous reflexes in the cat distal hindlimb and their gating during normal, treadmill walking. Soc Neurosci Abstr 13:1177
Loeb GE, Gans C (1986) Electromyography for experimentalists. University of Chicago Press, Chicago
Loeb GE, Levine WS, He J (1990) Understanding sensorimotor feedback through optimal control. Cold Spring Harb Symp Quant Biol 55:791–803
Loeb GE, Walmsley B, Duysens J (1980) Obtaining proprioceptive information from natural limbs: implantable transducers vs. somatosensory neuron recordings. In: Neuman MR (eds) Physical sensors for biomedical applications. (Proceedings of workshop on solid state physical sensors for biomedical application) CRC, Boca Raton, pp 135–149
Lundberg A (1975) Control of spinal mechanisms from the brain. In: Brady RO (eds) The nervous system, vol 1. Basic neuroscience. Raven, New York, pp 253–265
Lundberg A (1980) Half-centres revisited. Adv Physiol Sci 1:155–167
McMahon SB, Wall PD (1989) Changes in spinal cord reflexes after cross-anastomosis of cutaneous and muscle nerves in the adult rat. Nature 342:272–274
Merzenich MM, Grajski K (1990) Cortical network changes underlying representational plasticity. Cold Spring Harb Symp Quant Biol 55:873–887
Merzenich MM, Kaas JH, Wall J, Nelson RJ, Sur M, Felleman D (1983) Topographic reorganization of somato-sensory cortical areas 3B and 1 in adult monkeys following restricted deafferentation. Neuroscience 8:33–55
Miller S, Van der Burg J, Van der Meche FGA (1975) Coordination of movements of the hindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats. Brain Res 91:217–237
Moschovakis AK, Sholomenko GN, Burke RE (1991) Differential control of short latency cutaneous excitation in cat FDL motoneurons during fictive locomotion. Exp Brain Res 83:489–501
O'Donovan MJ, Pinter MJ, Dum RP, Burke RE (1982) Actions of FDL and FHL muscles in intact cats: functional dissociation between anatomical synergists. J Neurophysiol 47:1126–1143
Oguztoreli MN, Stein RB (1990) Optimal task performance of antagonistic muscles. Biol Cybern 64:87–94
Orlovsky GN, Shik ML (1976) Control of locomotion: a neurophysiological analysis of the cat locomotor system. Int Rev Physiol Neurophysiol 10:281–317
Pandy MG, Zajac FE, Sim E, Levine WS (1990) An optimal control model for maximum-height human jumping. J Biomech 23:1185–1198
Phillipson M (1905) L'autonomie et la centralisation dans le systeme nerveux des animaux. Trav Lab Physiol Inst Solvay (Bruxelles) 7:1–208
Pratt CA, Chanaud CM, Loeb GE (1991) Functionally complex muscles of the cat hindlimb. IV. Intramuscular distribution of movement command signals and cutaneous reflexes in broad, bifunctional thigh muscles. Exp Brain Res 85:281–299
Rindos AJ, Loeb GE, Levitan H (1984) Conduction velocity changes along lumbar primary afferent fibers in cats. Exp Neurol 86:208–226
Schmidt BJ, Meyers DER, Fleshman JW, Tokuriki M, Burke RE (1988) Phasic modulation of short latency cutaneous excitation in flexor digitorum longus motoneurons during fictive locomotion. Exp Brain Res 71:568–578
Schmidt BJ, Meyers DER, Tokuriki M, Burke R (1989) Modulation of short latency cutaneous excitation in flexor and extensor motoneurons during fictive locomotion in the cat. Exp Brain Res 77:57–68
Schomburg ED (1990) Spinal sensorimotor systems and their supraspinal control. Neurosci Res 7:265–340
Sherrington CS (1910) Flexion-reflex of the limb, crossed extensionreflex and reflex stepping and standing. J Physiol (Lond) 40:28–121
Sperry RW (1942) Transplantation of motor nerves and muscles in the forelimb of the rat. Neurology 76:283–321
Sperry RW (1945) The problem of central nervous reorganization after nerve regeneration and muscle transposition. Q Rev Biol 20:311–369
Sperry RW (1947) Effect of crossing nerves to antagonistic limb muscles in the monkey. Arch Neurol Psychiatry 58:452–473
Stein RB, Nichols TR, Jhamandas J, Davis L, Charles D (1977) Stable long-term recordings from cat peripheral nerves. Brain Res 128:21–38
Vilensky JA, Patrick MC (1984) Inter and intratrial variation in cat locomotion behavior. Physiol Behav 33:733–746
Wetzel MC, Atwater AE, Wait JV, Stuart DG (1975) Neural implications of different profiles between treadmill and overground locomotion timing in cats. J Neurophysiol 38:492–501
Wolpaw JR, Lee CE (1989) Memory traces in primate spinal cord produced by operant conditioning of H-reflex. J Neurophysiol 61:563–572
Young RP, Scott SH, Loeb GE (1992) An intrinsic mechanism to stablize posturejoint-angle-dependent moment arms of feline ankle muscles. Neurosci Lett 145:137–140
Young RP, Scott SH, Loeb GE (1993) The distal hindlimb muscularture of the cat: multiaxis moment arms at the ankle joint. Exp Brain Res 96:141–151
Yumiya H, Larsen KD, Asanuma H (1979) Motor readjustment and input-output relationship of motor cortex following crossconnection of forearm muscles in cats. Brain Res 177:566–570
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Loeb, G.E. The distal hindlimb musculature of the cat: interanimal variability of locomotor activity and cutaneous reflexes. Exp Brain Res 96, 125–140 (1993). https://doi.org/10.1007/BF00230446
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF00230446