Interlimb coordination during fictive locomotion in the thalamic cat

SummaryEfferent discharges in muscle nerves of the four limbs were recorded simultaneously during spontaneous fictive locomotion in thalamic cats with the goal of understanding how the central nervous system controls interlimb coordination during stepping. The onset of the bursts of activity in the nerve of a selected flexor muscle in each limb allowed the temporal and the phase relationships between the fictive step cycle of a pair of limbs to be determined. Our main results are the following: 1) the fictive step cycles of the two forelimbs are always strictly alternated whereas the phasing of the step cycles of either the two hindlimbs or pairs of homolateral or diagonal limbs is more variable; 2) the time interval between the onsets of the flexor bursts of one of the two pairs of diagonal limbs is independent of the step cycle duration; 3) distinct patterns of interlimb coordination exist during fictive locomotion; a small number of patterns of coordination involving all four limbs, which correspond to the walking and the trotting gaits in the intact cat, occur very frequently. The results demonstrate that the central nervous system deprived of phasic afferent inputs from the periphery has the capacity to generate most of the patterns of interlimb coordination which occur during real locomotion. They further support the view that the central pattern of interlimb coordination essentially results from diagonal interactions between a forelimb generator for locomotion and a hindlimb one.

[1]  Milton Hildebrand,et al.  Analysis of Tetrapod Gaits: General Considerations and Symmetrical Gaits , 1976 .

[2]  Mary C. Wetzel,et al.  Reinforcement influences upon topography of treadmill locomotion by cats , 1976, Physiology & Behavior.

[3]  C. Perret,et al.  Analysis of the Pattern of Activity in “Knee Flexor” Motoneurons During Locomotion in the Cat , 1988 .

[4]  C. Perret,et al.  Neural Control of Locomotion in the Decorticate Cat , 1976 .

[5]  S. Rossignol,et al.  Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat. , 1988, Journal of neurophysiology.

[6]  S. Grillner Control of Locomotion in Bipeds, Tetrapods, and Fish , 1981 .

[7]  J. Cabelguen,et al.  Main characteristics of the hindlimb locomotor cycle in the decorticate cat with special reference to bifunctional muscles , 1980, Brain Research.

[8]  S. Miller,et al.  Coordinated stepping of all four limbs in the high spinal cat , 1976, Brain Research.

[9]  O. I. Fukson,et al.  [Activity of neurons of the dorsal spinocerebellar tract during locomotion]. , 1972, Biofizika.

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

[11]  G. E. Goslow,et al.  Time Constraints for Inter-Limb Co-Ordination in the Cat During Unrestrained Locomotion , 1973 .

[12]  A. English Interlimb coordination during stepping in the cat: an electromyographic analysis. , 1979, Journal of neurophysiology.

[13]  Michael J. O'Donovan,et al.  Cat hindlimb motoneurons during locomotion. II. Normal activity patterns. , 1987, Journal of neurophysiology.

[14]  A. English,et al.  An electromyographic analysis of forelimb muscles during overground stepping in the cat. , 1978, The Journal of experimental biology.

[15]  S. Grillner,et al.  Central Generation of Locomotion in Vertebrates , 1976 .

[16]  M. Kato Chronically isolated lumbar half spinal cord, produced by hemisection and longitudinal myelotomy, generates locomotor activities of the ipsilateral hindlimb of the cat , 1989, Neuroscience Letters.

[17]  S. Rossignol,et al.  Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill. , 1986, Journal of neurophysiology.

[18]  J V Wait,et al.  Kinematics of locomotion by cats with a single hindlimb deafferented. , 1976, Journal of neurophysiology.

[19]  C. Perret Centrally generated pattern of motoneuron activity during locomotion in the cat. , 1983, Symposia of the Society for Experimental Biology.

[20]  O. I. Fukson,et al.  Recordings of neurones of the dorsal spinocerebellar tract during evoked locomotion. , 1972, Brain research.

[21]  D. Viala,et al.  Evidence for distinct spinal locomotion generators supplying respectively fore- and hindlimbs in the rabbit , 1978, Brain Research.

[22]  P. P. Gambari︠a︡n How mammals run : anatomical adaptations , 1974 .

[23]  S. Miller,et al.  Coordination of movements of the hindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats , 1975, Brain Research.

[24]  J. Cabelguen,et al.  Comparison between ventral spincocerebellar and rubrospinal activities during locomotion in the cat , 1988, Behavioural Brain Research.

[25]  A. G. Fel'dman,et al.  Role of afferent activity in the generation of stepping movements , 2005, Neurophysiology.

[26]  S. Grillner,et al.  On the central generation of locomotion in the low spinal cat , 1979, Experimental Brain Research.

[27]  J. Halbertsma,et al.  Basic Programs for the Phasing of Flexion and Extension Movements of the Limbs during Locomotion , 1976 .

[28]  J V Wait,et al.  Neural implications of different profiles between treadmill and overground locomotion timings in cats. , 1975, Journal of neurophysiology.

[29]  P. Zangger The effect of 4-aminopyridine on the spinal locomotor rhythm induced byl-DOPA , 1981, Brain Research.

[30]  Yu. I. Arshavskii,et al.  Activity of propriospinal neurons in segments C3 and C4 during fictitious locomotion in cats , 2005, Neurophysiology.

[31]  P. Buser,et al.  Activits locomotrices rythmiques strotypes chez le lapin sous anesthsie lgre: Etude de leurs caractristiques gnrales , 1969 .

[32]  S. Miller,et al.  The Function of Long Propriospinal Pathways in the Co-Ordination of Quadrupedal Stepping in the Cat , 1973 .

[33]  Longitudinal myelotomy of lumbar spinal cord has little effect on coordinated locomotor activities of bilateral hindlimbs of the chronic cats , 1988, Neuroscience Letters.

[34]  S. Grillner Locomotion in vertebrates: central mechanisms and reflex interaction. , 1975, Physiological reviews.

[35]  J. Massion,et al.  The placing reaction in the standing cat: A model for the study of posture and movement , 1979, Experimental Brain Research.

[36]  P. Buser,et al.  [Stereotyped rhythmic motor activities in the rabbit. A study of their general characteristics]. , 1969, Experimental brain research.

[37]  Serge Rossignol,et al.  The effects of 4-aminopyridine on the spinal cord: Rhythmic discharges recorded from the peripheral nerves , 1986, Brain Research.

[38]  J. Cabelguen,et al.  Evidence of rhythmic inhibitory synaptic influences in hindlimb motoneurons during fictive locomotion in the thalamic cat , 2004, Experimental Brain Research.

[39]  Y. Arshavsky,et al.  Activity of rubrospinal neurons during locomotion and scratching in the cat , 1988, Behavioural Brain Research.

[40]  M. L. Shik,et al.  [Control of walking and running by means of electric stimulation of the midbrain]. , 1966, Biofizika.

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

[42]  J. Cabelguen,et al.  CENTRAL PATTERN GENERATION OF FORELIMB AND HINDLIMB LOCOMOTOR ACTIVITIES IN THE CAT , 1981 .

[43]  J. Gray Studies in the Mechanics of the Tetrapod Skeleton , 1944 .

[44]  Y. Arshavsky,et al.  Cerebellum and Rhythmical Movements , 1986 .

[45]  J. Halbertsma The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic recordings. , 1983, Acta physiologica Scandinavica. Supplementum.

[46]  A. English Interlimb coordination during stepping in the cat: effects of dorsal column section. , 1980, Journal of neurophysiology.

[47]  S. Miller,et al.  Functional organization of long ascending propriospinal pathways linking lumbo-sacral and cervical segments in the cat. , 1973, Brain research.

[48]  S. Rossignol,et al.  The locomotion of the low spinal cat. II. Interlimb coordination. , 1980, Acta physiologica Scandinavica.

[49]  Action of muscular group III and IV afferents on spinal locomotor activity in cat , 1980, Brain Research.

[50]  E. Schomburg,et al.  Phasic modulation of trunk muscle efferents during fictive spinal locomotion in cats. , 1984, The Journal of physiology.

[51]  H. Steffens,et al.  Effects from fine muscle and cutaneous afferents on spinal locomotion in cats , 1981, The Journal of physiology.

[52]  D. Marsh,et al.  Role of afferent activity from the bladder in regulating its activity. , 1959, American Journal of Physiology.

[53]  E. Schomburg,et al.  Changes in segmental and propriospinal reflex pathways during spinal locomotion , 1981 .

[54]  Shik Ml,et al.  Control of walking and running by means of electrical stimulation of the mesencephalon. , 1969 .

[55]  S. Miller,et al.  Locomotion in the cat: Basic programmes of movement , 1975, Brain Research.

[56]  P. R. Lennard,et al.  Interlimb coordination during stepping in the cat: In-phase stepping and gait transitions , 1982, Brain Research.