Adaptive changes in motor activity associated with functional recovery following muscle denervation in walking cats.

In this investigation we examined the changes in the pattern of activity in the medial gastrocnemius (MG) muscle in walking cats following transection of the nerves innervating synergist muscles (lateral gastrocnemius, soleus, and plantaris). Immediately following the nerve transections, there was a large increase in ankle flexion during early stance (from approximately 10 to approximately 30 degrees ) and a marked increase in the magnitude of the MG bursts during stance. We attribute this increase in the magnitude of the MG bursts to an increase in afferent feedback from the abnormally stretched MG muscle. During the week after the nerve transections, there was a progressive decrease in ankle yield. This improvement in ankle function was correlated with an increase in magnitude of two components of the MG bursts; the initial component starting during late swing and ending approximately 40 ms after ground contact, and a late component associated with stance. The time courses of the increases in the initial and late components of the MG bursts were different. Large and significant increases in the late component occurred the day after the nerve transections, whereas increases in the initial component occurred more gradually. This difference in time course was reflected in the kinematics of ankle movement. Over the first few days after the nerve transections, improvement in ankle movement occurred primarily late in the stance phase, and there was little change in ankle yield during early stance. At 1 wk, however, there was a significant reduction in ankle yield during early stance. This decreased yield was most likely due to an increase in stiffness of the MG muscle at the time of ground contact resulting from the increase in magnitude of the initial component of the MG bursts. The increases in the magnitude of the initial and late components of the MG bursts, as well as the improvement in ankle function, depended on use of the leg. All these changes were delayed by immobilizing the leg for 6 days in an extended position. We discuss possible mechanisms underlying the increase in the magnitude of the MG bursts and propose that proprioceptive signals from the stretched MG muscles provide an error signal for rescaling the magnitude of the centrally generated initial component. Our data support the concept that proprioceptive feedback functions to scale the magnitude of feed-forward motor commands to ensure they are appropriate for the biomechanical properties of the musculoskeletal system.

[1]  S. Grillner The role of muscle stiffness in meeting the changing postural and locomotor requirements for force development by the ankle extensors. , 1972, Acta physiologica Scandinavica.

[2]  M C Wetzel,et al.  Behavior and histochemistry of functionally isolated cat ankle extensors. , 1973, Experimental neurology.

[3]  G. E. Goslow,et al.  The cat step cycle: Hind limb joint angles and muscle lengths during unrestrained locomotion , 1973, Journal of morphology.

[4]  W. Rymer,et al.  Effect of compensatory hypertrophy studied in individual motor units in medial gastrocnemius muscle of the cat. , 1978, Journal of neurophysiology.

[5]  R. Gallego,et al.  Disuse enhances synaptic efficacy in spinal mononeurones. , 1979, The Journal of physiology.

[6]  L. Optican,et al.  Cerebellar-dependent adaptive control of primate saccadic system. , 1980, Journal of neurophysiology.

[7]  S. Grillner,et al.  The locomotion of the low spinal cat. I. Coordination within a hindlimb. , 1980, Acta physiologica Scandinavica.

[8]  S. Andreassen,et al.  Regulation of soleus muscle stiffness in premammillary cats: intrinsic and reflex components. , 1981, Journal of neurophysiology.

[9]  R. J. Gregor,et al.  Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat , 1986, Experimental Neurology.

[10]  S. Rossignol,et al.  Recovery of locomotion after chronic spinalization in the adult cat , 1987, Brain Research.

[11]  S G Lisberger,et al.  The neural basis for learning of simple motor skills. , 1988, Science.

[12]  M. Kawato,et al.  The cerebellum and VOR/OKR learning models , 1992, Trends in Neurosciences.

[13]  K. Pearson,et al.  Reversal of the influence of group Ib afferents from plantaris on activity in medial gastrocnemius muscle during locomotor activity. , 1993, Journal of neurophysiology.

[14]  M. Udo,et al.  A new learning paradigm: adaptive changes in interlimb coordination during perturbed locomotion in decerebrate cats , 1993, Neuroscience Research.

[15]  M. Gorassini,et al.  Corrective responses to loss of ground support during walking. I. Intact cats. , 1994, Journal of neurophysiology.

[16]  K. Pearson,et al.  Corrective responses to loss of ground support during walking. II. Comparison of intact and chronic spinal cats. , 1994, Journal of neurophysiology.

[17]  K. Pearson Proprioceptive regulation of locomotion , 1995, Current Opinion in Neurobiology.

[18]  R L Sainburg,et al.  Control of limb dynamics in normal subjects and patients without proprioception. , 1995, Journal of neurophysiology.

[19]  E. Knudsen,et al.  Creating a unified representation of visual and auditory space in the brain. , 1995, Annual review of neuroscience.

[20]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[21]  K. Pearson,et al.  Plasticity of the extensor group I pathway controlling the stance to swing transition in the cat. , 1995, Journal of neurophysiology.

[22]  T. Sejnowski,et al.  Learning and memory in the vestibulo-ocular reflex. , 1995, Annual review of neuroscience.

[23]  D. McCrea,et al.  Ankle extensor group I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. , 1995, The Journal of physiology.

[24]  W. T. Thach,et al.  Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. , 1996, Brain : a journal of neurology.

[25]  E Bizzi,et al.  Motor learning by field approximation. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Wise,et al.  The Acquisition of Motor Behavior in Vertebrates , 1996 .

[27]  S G Lisberger,et al.  Motor Learning and Memory in the Vestibulo‐Ocular Reflex: The Dark Side , 1996, Annals of the New York Academy of Sciences.

[28]  Michael I. Jordan Chapter 2 Computational aspects of motor control and motor learning , 1996 .

[29]  K. G. Pearson,et al.  Comparison of the effects of stimulating extensor group I afferents on cycle period during walking in conscious and decerebrate cats , 1997, Experimental Brain Research.

[30]  K. Pearson,et al.  Modification of group I field potentials in the intermediate nucleus of the cat spinal cord after chronic axotomy of an extensor nerve , 1997, Neuroscience Letters.

[31]  S. Rossignol,et al.  Locomotion of the hindlimbs after neurectomy of ankle flexors in intact and spinal cats: model for the study of locomotor plasticity. , 1997, Journal of neurophysiology.

[32]  D. Feldman,et al.  An Anatomical Basis for Visual Calibration of the Auditory Space Map in the Barn Owl’s Midbrain , 1997, The Journal of Neuroscience.

[33]  V R Edgerton,et al.  Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. , 1998, Journal of neurophysiology.

[34]  D. Wolpert,et al.  Temporal and amplitude generalization in motor learning. , 1998, Journal of neurophysiology.

[35]  K. Pearson,et al.  Contribution of sensory feedback to the generation of extensor activity during walking in the decerebrate Cat. , 1999, Journal of neurophysiology.

[36]  Tamar Flash,et al.  Computational approaches to motor control , 2001, Current Opinion in Neurobiology.