Reciprocal Ia inhibition contributes to motoneuronal hyperpolarisation during the inactive phase of locomotion and scratching in the cat

During a movement, the contraction of a given muscle group is often coordinated with the simultaneous relaxation of its antagonist muscles. The neural basis of this antagonist relaxation has been investigated in both animal and human experiments for decades and it is believed that activation of the Ia inhibitory interneurones by central motor programmes plays a major role in this relaxation of antagonist muscles. The alternating movements during locomotion would seem to especially require reciprocal actions, but recent studies have raised significant questions about the role of this inhibition. We found that inhibition evoked by these inhibitory interneurones is largest when their target motoneurones are inactive – even in the absence of supraspinal influence. The results of this work provide new evidence for the role of the Ia inhibitory interneurones during rhythmic motor activity. This supports the classical view of reciprocal inhibition as a basis for antagonist relaxation.

[1]  Loyal Davis,et al.  The reflex activities of a decerebrate animal , 1930 .

[2]  J. Eccles,et al.  The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post‐synaptic potential , 1955, The Journal of physiology.

[3]  J. Eccles,et al.  Central pathway for direct inhibitory action of impulses in largest afferent nerve fibres to muscle. , 1956, Journal of neurophysiology.

[4]  A. Lundberg,et al.  Integrative pattern of Ia synaptic actions on motoneurones of hip and knee muscles , 1958, The Journal of physiology.

[5]  J. Eccles,et al.  The time courses of excitatory and inhibitory synaptic actions , 1959, The Journal of physiology.

[6]  W. Feldberg,et al.  Scratching movements and facilitation of the scratch reflex produced by tubocurarine in cats , 1960, The Journal of physiology.

[7]  R E Burke,et al.  Motor unit types of cat triceps surae muscle , 1967, The Journal of physiology.

[8]  R E Burke,et al.  Firing patterns of gastrocnemius motor units in the decerebrate cat , 1968, The Journal of physiology.

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

[10]  M. L. Shik,et al.  Control of walking and running by means of electrical stimulation of the mesencephalon. , 1969, Electroencephalography and clinical neurophysiology.

[11]  H. Hultborn,et al.  Recurrent inhibition of interneurones monosynaptically activated from group Ia afferents , 1971, The Journal of physiology.

[12]  R. Burke,et al.  Electrotonic characteristics of alpha motoneurones of varying size , 1971, The Journal of physiology.

[13]  E Jankowska,et al.  Synaptic actions of single interneurones mediating reciprocal Ia inhibition of motoneurones , 1972, The Journal of physiology.

[14]  G. Orlovsky Activity of rubrospinal neurons during locomotion. , 1972, Brain research.

[15]  G. Orlovsky,et al.  Activity of vestibulospinal neurons during locomotion. , 1972, Brain research.

[16]  H Hultborn,et al.  Convergence on interneurones in the reciprocal Ia inhibitory pathway to motoneurones. , 1972, Acta physiologica Scandinavica. Supplementum.

[17]  G. Orlovsky,et al.  Activity of interneurons mediating reciprocal 1a inhibition during locomotion , 1975, Brain Research.

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

[19]  G. Orlovsky,et al.  Messages conveyed by descending tracts during scratching in the cat. II. Activity of rubrospinal neurons , 1978, Brain Research.

[20]  Y. Arshavsky,et al.  Messages conveyed by descending tracts during scratching in the cat. I. Activity of vestibulospinal neurons , 1978, Brain Research.

[21]  G. Orlovsky,et al.  Activity of motoneurons during fictitious scratch reflex in the cat , 1980, Brain Research.

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

[23]  G. Orlovsky,et al.  Activity of Ia inhibitory interneurons during fictitious scratch reflex in the cat , 1980, Brain Research.

[24]  L. Kempe Handbook of Physiology. Section I. The Nervous System , 1982 .

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

[26]  Y. Arshavsky,et al.  The cerebellum and control of rhythmical movements , 1983, Trends in Neurosciences.

[27]  L. Jordan,et al.  Excitatory and inhibitory postsynaptic potentials in alpha-motoneurons produced during fictive locomotion by stimulation of the mesencephalic locomotor region. , 1985, Journal of neurophysiology.

[28]  L. Jordan,et al.  Motoneuron input-resistance changes during fictive locomotion produced by stimulation of the mesencephalic locomotor region. , 1985, Journal of neurophysiology.

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

[30]  C. Pratt,et al.  Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion. , 1987, Journal of neurophysiology.

[31]  H. Hultborn,et al.  Reciprocal Ia inhibition between ankle flexors and extensors in man. , 1987, The Journal of physiology.

[32]  H. Wigström,et al.  Maintained changes in motoneuronal excitability by short‐lasting synaptic inputs in the decerebrate cat. , 1988, The Journal of physiology.

[33]  G. A. Robertson,et al.  Synaptic control of hindlimb motoneurones during three forms of the fictive scratch reflex in the turtle. , 1988, The Journal of physiology.

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

[35]  C. Crone,et al.  Spinal mechanisms in man contributing to reciprocal inhibition during voluntary dorsiflexion of the foot. , 1989, The Journal of physiology.

[36]  S J Redman,et al.  Voltage dependence of Ia reciprocal inhibitory currents in cat spinal motoneurones. , 1990, The Journal of physiology.

[37]  J. Nielsen,et al.  The regulation of disynaptic reciprocal Ia inhibition during co‐contraction of antagonistic muscles in man. , 1992, The Journal of physiology.

[38]  S. Rossignol,et al.  Activity of medullary reticulospinal neurons during fictive locomotion. , 1993, Journal of neurophysiology.

[39]  D J Kriellaars,et al.  Mechanical entrainment of fictive locomotion in the decerebrate cat. , 1994, Journal of neurophysiology.

[40]  S. Grillner,et al.  Neuronal Control of Locomotion 'From Mollusc to Man ' , 1999 .

[41]  H. Hultborn,et al.  Proprioceptive Control of Extensor Activity during Fictive Scratching and Weight Support Compared to Fictive Locomotion , 1999, The Journal of Neuroscience.

[42]  S. Grillner,et al.  Neuronal Control of LocomotionFrom Mollusc to Man , 1999 .

[43]  N. Petersen,et al.  Modulation of reciprocal inhibition between ankle extensors and flexors during walking in man , 1999, The Journal of physiology.

[44]  M. Perreault Motoneurons Have Different Membrane Resistance during Fictive Scratching and Weight Support , 2002, The Journal of Neuroscience.

[45]  H Hultborn,et al.  Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current , 2003, The Journal of physiology.

[46]  J. Nielsen,et al.  Changes in reciprocal inhibition across the ankle joint with changes in external load and pedaling rate during bicycling. , 2003, Journal of neurophysiology.

[47]  K. Pearson,et al.  Entrainment of the locomotor rhythm by group Ib afferents from ankle extensor muscles in spinal cats , 2004, Experimental Brain Research.

[48]  R. Tanaka,et al.  Reciprocal Ia inhibition during voluntary movements in man , 1974, Experimental Brain Research.

[49]  A. Lundberg,et al.  The rubrospinal tract. II. Facilitation of interneuronal transmission in reflex paths to motoneurones , 1969, Experimental Brain Research.

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

[51]  H. Hultborn,et al.  Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat , 2004, Experimental Brain Research.

[52]  J. Nielsen,et al.  Sensitivity of monosynaptic test reflexes to facilitation and inhibition as a function of the test reflex size: a study in man and the cat , 2004, Experimental Brain Research.

[53]  Activity of lumbosacral interneurons during fictitious scratching , 2005, Neurophysiology.

[54]  J. Hounsgaard,et al.  Periodic High-Conductance States in Spinal Neurons during Scratch-Like Network Activity in Adult Turtles , 2005, The Journal of Neuroscience.

[55]  Rune W. Berg,et al.  Balanced Inhibition and Excitation Drive Spike Activity in Spinal Half-Centers , 2007, Science.

[56]  J. Valls-Solé The circuitry of the human spinal cord: Its role in motor control and movement disorders Pierrot-Deseilligny E, Burke D, editors. Hardback. Cambridge University Press; 2005. 642 p. [ISBN: 13978052182581]. , 2008, Clinical Neurophysiology.

[57]  G. Drummond Reporting ethical matters in The Journal of Physiology: standards and advice , 2009, The Journal of physiology.

[58]  P. Stein,et al.  Alternation of agonists and antagonists during turtle hindlimb motor rhythms , 2010, Annals of the New York Academy of Sciences.

[59]  H. Hultborn,et al.  Integration in Spinal Neuronal Systems , 2011 .