Developmental Adaptation of Rat Nociceptive Withdrawal Reflexes after Neonatal Tendon Transfer

Nociceptive withdrawal reflexes (NWRs) were studied in adult rats in which the movement patterns produced by single muscles had been altered by neonatal tendon transfer. NWRs evoked by cutaneous noxious mechanical and thermal (CO2-laser) stimulation were recorded using electromyography in a decerebrate spinal preparation. The sensitivity distribution within the receptive fields of the NWRs of the extensor digitorum longus and the peronei muscles exhibited changes corresponding to the altered movement patterns. No detectable change of NWRs was found in normal muscles whose receptive fields overlapped that of the modified muscle. Furthermore, NWRs of muscles that regained an essentially normal function after neonatal tendon transfer did not differ from normal. It is proposed that a developmental experience-dependent mechanism, which takes into account the hindlimb movement pattern caused by contraction of single muscles, underlies the functionally adapted organization of adult NWRs.

[1]  C. Sherrington.  Flexion‐reflex of the limb, crossed extension‐reflex, and reflex stepping and standing , 1910, The Journal of physiology.

[2]  F. V. Abbott,et al.  The behavioral response to formalin in preweanling rats , 1992, Pain.

[3]  Joseph S. Edwards,et al.  Fetal Movement: Development and Time Course , 1970, Science.

[4]  J. Ekholm.  Postnatal changes in cutaneous reflexes and in the discharge pattern of cutaneous and articular sense organs. A morphological and physiological study in the cat. , 1967, Acta physiologica Scandinavica. Supplementum.

[5]  P. Redfern.  Neuromuscular transmission in new‐born rats , 1970, The Journal of physiology.

[6]  J. Schouenborg,et al.  Developmental adaptation of withdrawal reflexes to early alteration of peripheral innervation in the rat. , 1996, The Journal of physiology.

[7]  J Schouenborg,et al.  Modular Organization of Spinal Nociceptive Reflexes: A New Hypothesis , 1994 .

[8]  K. Walton,et al.  Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. , 1991, The Journal of physiology.

[9]  Hagbarth Ke.  Excitatory and inhibitory skin areas for flexor and extensor motoneurons. , 1952 .

[10]  E. Kandel,et al.  Differential classical conditioning of a defensive withdrawal reflex in Aplysia californica. , 1983, Science.

[11]  J. Willer,et al.  Comparative study of perceived pain and nociceptive flexion reflex in man , 1977, Pain.

[12]  M. Pillai,et al.  Are the behavioural states of the newborn comparable to those of the fetus? , 1990, Early human development.

[13]  J. Schouenborg,et al.  Topography and nociceptive receptive fields of climbing fibres projecting to the cerebellar anterior lobe in the cat. , 1991, The Journal of physiology.

[14]  M. Fitzgerald.  Prenatal growth of fine‐diameter primary afferents into the rat spinal cord: A transganglionic tracer study , 1987, The Journal of comparative neurology.

[15]  G. Grant,et al.  Laminar distribution and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidase in the rat , 1986, Neuroscience.

[16]  J. Changeux,et al.  Consequences of tenotomy on the evolution of multiineervation in developing rat soleus muscle , 1975, Brain Research.

[17]  A. Gonźlez,et al.  The prenatal development of behavior in the albino rat , 1932 .

[18]  C. Bennett-Clarke,et al.  Peripheral influences on the size and organization of somatotopic representations in the fetal rat cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  M. Koltzenburg,et al.  The functional development of descending inhibitory pathways in the dorsolateral funiculus of the newborn rat spinal cord. , 1986, Brain research.

[20]  Bradley L. Schlaggar,et al.  Postsynaptic control of plasticity in developing somatosensory cortex , 1993, Nature.

[21]  M. Fitzgerald.  Spontaneous and evoked activity of fetal primary afferents in vivo , 1987, Nature.

[22]  J Schouenborg,et al.  Postnatal development of the nociceptive withdrawal reflexes in the rat: a behavioural and electromyographic study. , 1996, The Journal of physiology.

[23]  B. Matthews,et al.  The thresholds of the jaw-opening reflex and trigeminal brainstem neurons to tooth-pulp stimulation in acutely and chronically prepared cats , 1990, Neuroscience.

[24]  K. Hagbarth.  Excitatory and inhibitory skin areas for flexor and extensor motoneurons. , 1952, Acta physiologica Scandinavica. Supplementum.

[25]  M. Constantine-Paton,et al.  N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[26]  E. Fleischer,et al.  Unmyelinated nociceptive units in two skin areas of the rat , 1983, Brain Research.

[27]  M. Merzenich,et al.  Reorganization of cortical representations of the hand following alterations of skin inputs induced by nerve injury, skin island transfers, and experience. , 1993, Journal of hand therapy : official journal of the American Society of Hand Therapists.

[28]  Carolyn L. Smith.  The development and postnatal organization of primary afferent projections to the rat thoracic spinal cord , 1983, The Journal of comparative neurology.

[29]  W. Singer.  Ontogenetic self-organization and learning. , 1990 .

[30]  R. Schmidt,et al.  Responsiveness of the somatosensory system after nerve injury and amputation in the human hand , 1994, Annals of neurology.

[31]  M. Fitzgerald.  Cutaneous primary afferent properties in the hind limb of the neonatal rat. , 1987 .

[32]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  E. Knudsen.  Experience alters the spatial tuning of auditory units in the optic tectum during a sensitive period in the barn owl , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  F. Benedetti,et al.  The Effects of Early Postnatal Modification of Body Shape on the Somatosensory—Visual Organization in Mouse Superior Colliculus , 1995, The European journal of neuroscience.

[35]  J. Swett,et al.  The termination pattern of sciatic nerve afferents in the substantia gelatinosa of neonatal rats , 1983, Neuroscience Letters.

[36]  A. J. Scheetz,et al.  Modulation of NMDA receptor function: implications for vertebrate neural development , 1994, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[37]  D. J. Felleman,et al.  Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation , 1983, Neuroscience.

[38]  V. Hamburger,et al.  Prenatal development of spontaneous and evoked activity in the rat (Rattus norvegicus albinus). , 1971, Behaviour.

[39]  H. Killackey,et al.  Expansion of the Central Hindpaw Representation Following Fetal Forelimb Removal in the Rat , 1989, The European journal of neuroscience.

[40]  V. Hamburger.  Embryonic Motility in Vertebrates , 1970 .

[41]  R. Miledi,et al.  Electrical synapses between motoneurons in the spinal cord of the newborn rat , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[42]  J. Schouenborg,et al.  Differential Effects of a Distant Noxious Stimulus on Hindlimb Nociceptive Withdrawal Reflexes in the Rat , 1992, The European journal of neuroscience.

[43]  H. Asanuma,et al.  Relationship between afferent input and motor outflow in cat motorsensory cortex. , 1968, Journal of neurophysiology.

[44]  J. Kaas,et al.  Large-scale functional reorganization in adult monkey cortex after peripheral nerve injury. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[45]  W D Willis,et al.  Cutaneous sensory receptors in the rat foot. , 1993, Journal of neurophysiology.

[46]  E. Perl,et al.  Cutaneous Sensory Receptors , 1994, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.