H reflex restitution and facilitation after different types of peripheral nerve injury and repair

This study addresses the restitution of monosynaptic H reflex after nerve injuries and their role in the recovery of walking. Adult rats were submitted to sciatic crush, complete section repaired by aligned or crossed fascicular suture, or an 8-mm resection repaired by autograft or tube repair. The sciatic nerve was stimulated proximal to the injury site and the M and H waves were recorded from gastrocnemius (GCm) and plantar (PLm) muscles at monthly intervals during 3 months postoperation. Walking track tests were also carried out and the sciatic functional index (SFI) calculated to assess gait recovery. The M and H waves reappeared in all the animals at the end of the follow-up. The H/M amplitude ratio increased during the first stages of regeneration and tended to decrease to control values as muscle reinnervation progressed. However, final values of the H/M ratio for the PLm remained significantly higher in all the groups except that with a nerve crush. The walking track pattern showed an appreciable recovery only after crush injury. Final SFI values correlated positively with the M wave amplitude and negatively with the H/M ratio. In conclusion, H reflex is facilitated after peripheral nerve injury and regeneration and tends to return to normal excitability with time. Changes in the H reflex circuitry and excitability correlated positively with the deficient recovery of walking pattern after severe nerve injury.

[1]  F. Rodrı́guez,et al.  Ensheathing glia transplants promote dorsal root regeneration and spinal reflex restitution after multiple lumbar rhizotomy , 1999, Annals of neurology.

[2]  M. Devor,et al.  Extent of fiber regeneration after peripheral nerve repair: Silicone splint vs. suture, gap repair vs. graft , 1987, Experimental Neurology.

[3]  T. A. Abelew,et al.  Local loss of proprioception results in disruption of interjoint coordination during locomotion in the cat. , 2000, Journal of neurophysiology.

[4]  H. Schmalbruch,et al.  Fiber composition of the rat sciatic nerve , 1986, The Anatomical record.

[5]  L. Mendell Modifiability of spinal synapses. , 1984, Physiological reviews.

[6]  R. L. Holland,et al.  An assessment of the spread of the signal for terminal sprouting within and between muscles , 1981, Brain Research.

[7]  Limited plasticity of adult motor units conserves recruitment order and rate coding. , 1999, Progress in brain research.

[8]  D. Ceballos,et al.  Improvement of regeneration with predegenerated nerve transplants in silicone chambers. , 1999, Restorative neurology and neuroscience.

[9]  I. Tavares,et al.  GABA decreases in the spinal cord dorsal horn after peripheral neurectomy , 1993, Brain Research.

[10]  L. D. Medinaceli Functional consequences of experimental nerve lesions: Effects of time, location, and extent of damage , 1988, Experimental Neurology.

[11]  P. Thomas,et al.  Neurotropic influence of the distal stump of transected peripheral nerve on axonal regeneration: absence of topographic specificity in adult nerve. , 1992, Journal of anatomy.

[12]  S. Mackinnon,et al.  Selective reinnervation: a comparison of recovery following microsuture and conduit nerve repair , 1991, Brain Research.

[13]  R. Coggeshall,et al.  Preservation of sensory cells by placing stumps of transected nerve in an impermeable tube , 1989, Experimental Neurology.

[14]  R. Blanks,et al.  Motoneurons of the rat sciatic nerve , 1986, Experimental Neurology.

[15]  J. Hellgren,et al.  A physiological study of the monosynaptic reflex responses of cat spinal α-motoneurons after partial lumbosacral deafferentation , 1989, Brain Research.

[16]  C. Pratt,et al.  Renshaw cell activity and recurrent effects on motoneurons during fictive locomotion. , 1980, Journal of neurophysiology.

[17]  J. Kellerth,et al.  Restorative effects of reinnervation on the size and dendritic arborization patterns of axotomized cat spinal α‐motoneurons , 1992, The Journal of comparative neurology.

[18]  H. Koerber,et al.  Central sprouting and functional plasticity of regenerated primary afferents , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  J. Swett,et al.  All peroneal motoneurons of the rat survive crush injury but some fail to reinnervate their original targets , 1991, The Journal of comparative neurology.

[20]  B LIBET,et al.  The behaviour of chromatolysed motoneurones studied by intracellular recording , 1958, The Journal of physiology.

[21]  P. Reier,et al.  Altered patterns of reflex excitability subsequent to contusion injury of the rat spinal cord. , 1992, Journal of neurophysiology.

[22]  The static sensitivity of tendon organs during recovery from nerve injury , 1995, Brain Research.

[23]  J. Kellerth,et al.  Changes in size and dendritic arborization patterns of adult cat spinal α‐Motoneurons following permanent axotomy , 1992, The Journal of comparative neurology.

[24]  Anatol G. Feldman,et al.  The role of stretch reflex threshold regulation in normal and impaired motor control , 1994, Brain Research.

[25]  X. Navarro,et al.  Comparison of Regenerative and Reinnervating Capabilities of Different Functional Types of Nerve Fibers , 1994, Experimental Neurology.

[26]  J. Scott Regeneration of gamma-fusimotor axons after nerve-freeze injury in the cat , 1985, Brain Research.

[27]  T. Nichols,et al.  Reinnervated muscles fail to produce stretch reflexes. , 1994, Journal of neurophysiology.

[28]  W. Freed,et al.  An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks , 1982, Experimental Neurology.

[29]  T. Cope,et al.  Motor-unit recruitment in self-reinnervated muscle. , 1993, Journal of neurophysiology.

[30]  X. Navarro,et al.  Comparison of Immunohistochemical and Functional Reinnervation of Skin and Muscle after Peripheral Nerve Injury , 1997, Experimental Neurology.

[31]  M. Desantis,et al.  Location and completeness of reinnervation by two types of neurons at a single target: The feline muscle spindle , 1993, The Journal of comparative neurology.

[32]  G. Panesar,et al.  Small-signal sensitivity of muscle spindles reinnervated after long-term denervation , 1995, Brain Research.

[33]  S. McMahon,et al.  Physiological properties of primary sensory neurons appropriately and inappropriately innervating skeletal muscle in adult rats. , 1991, Journal of neurophysiology.

[34]  J. Munson,et al.  Retrograde effects on synaptic transmission at the Ia/motoneuron connection , 1999, Journal of Physiology-Paris.

[35]  L C Katz,et al.  Neurotrophins and synaptic plasticity. , 1999, Annual review of neuroscience.

[36]  S. Sunderland Factors influencing the course of regeneration and the quality of the recovery after nerve suture. , 1952, Brain : a journal of neurology.

[37]  M. Botte,et al.  Inaccurate projection of rat soleus motoneurons: A comparison of nerve repair techniques , 1997, Muscle & nerve.

[38]  R. Coggeshall,et al.  Peripheral nerve injury triggers central sprouting of myelinated afferents , 1992, Nature.

[39]  Göran Lundborg,et al.  Spatial‐Temporal progress of peripheral nerve regeneration within a silicone chamber: Parameters for a bioassay , 1983, The Journal of comparative neurology.

[40]  A. Valero-Cabré,et al.  Superior muscle reinnervation after autologous nerve graft or poly‐L‐lactide‐ϵ‐caprolactone (PLC) tube implantation in comparison to silicone tube repair , 2001, Journal of neuroscience research.

[41]  S. Mackinnon,et al.  Functional Evaluation of Complete Sciatic, Peroneal, and Posterior Tibial Nerve Lesions in the Rat , 1989, Plastic and reconstructive surgery.

[42]  R. Sidman,et al.  Nerve Regeneration through Synthetic Biodegradable Nerve Guides: Regulation by the Target Organ , 1984, Plastic and reconstructive surgery.

[43]  Stanley J. Wiegand,et al.  The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons , 1992, Neuron.

[44]  M. Fitzgerald,et al.  Neonatal Sciatic Nerve Section Results in a Rearrangement of the Central Terminals of Saphenous and Axotomized Sciatic Nerve Afferents in the Dorsal Horn of the Spinal Cord of the Adult Rat , 1994, The European journal of neuroscience.

[45]  H. Meinck Occurrence of the H reflex and the F wave in the rat. , 1976, Electroencephalography and clinical neurophysiology.

[46]  H Hultborn,et al.  Distribution of recurrent inhibition within a motor nucleus. I. Contribution from slow and fast motor units to the excitation of Renshaw cells. , 1988, Acta physiologica Scandinavica.

[47]  M. Fisher AAEM minimonograph #13: H reflexes and F waves: Physiology and clinical indications , 1992, Muscle & nerve.

[48]  K. Ossowska,et al.  The influence of dizocilpine (MK-801) on the reserpine-enhanced electromyographic stretch reflex in rats , 1996, Neuroscience Letters.

[49]  Functional consequences of experimental nerve lesions: Effects of reinnervation blend , 1988, Experimental Neurology.

[50]  A. Gramsbergen,et al.  Sciatic Nerve Transection in the Adult Rat: Abnormal EMG Patterns during Locomotion by Aberrant Innervation of Hindleg Muscles , 2000, Experimental Neurology.

[51]  L. Guttmann,et al.  FACTORS AFFECTING RECOVERY OF SENSORY FUNCTION AFTER NERVE LESIONS , 1942 .

[52]  P. Sanna,et al.  Presumptive Renshaw cells contain decreased calbindin during recovery from sciatic nerve lesions. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[53]  K. Horch,et al.  Changes in primary afferent depolarization of sensory neurones during peripheral nerve regeneration in the cat. , 1981, The Journal of physiology.

[54]  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.

[55]  R. Stein,et al.  Pattern of recruiting human motor units in neuropathies and motor neurone disease , 1974, Journal of neurology, neurosurgery, and psychiatry.

[56]  M. Graeber,et al.  Delayed astrocyte reaction following facial nerve axotomy , 1988, Journal of neurocytology.