Recovery of function after spinal cord hemisection in newborn and adult rats: Differential effects on reflex and locomotor function

It is often assumed that the response of the immature nervous system to injury is more robust and exhibits greater anatomical reorganization and greater recovery of function than in the adult. In the present experiments the extent of recovery of function after spinal cord injury at birth or at maturity was assessed. We used a series of quantitative tests of motor behavior to measure reflex responses and triggered movements and to examine different components of locomotion. Rats received a midthoracic "over-hemisection" at birth or as adults. The neonatal operates were allowed to mature and the adult operates were allowed to recover. The animals were trained to walk on a treadmill and to cross runways of varying difficulty. The animals were tested for reflex responses and triggered movements, videotaped while crossing the runways, and footprinted while walking on the treadmill. The adult operates had greater deficits in the reflex responses than the neonatal operates. The adult operates lost the contact placing response and had a decreased hopping response in the ipsilateral limb, while these responses were not impaired in the neonatal operates. Although the contact placing response in the neonatal operates was spared, a greater stimulus was necessary to induce the response than in control animals. In contrast, the neonatal operates had greater deficits in locomotion. Footprint analysis revealed that the animals' base of support was significantly greater after the neonatal injury than after the adult injury, and deficits in limb rotation were larger in the neonatal operates than in the adult operates. Both groups crossed the grid with a similar number of steps but the adult operates made significantly more errors with the hindlimb ipsilateral to the lesion than the contralateral one, while the neonatal operates made an equivalent number of errors with both limbs. The neonatal operates took longer to execute the climb test and used a different movement pattern than the adult operates. The neonatal operates had a different locomotor pattern than the adult operates. Despite greater recovery of reflex responses after spinal cord injury at birth, the pattern of locomotion exhibits greater deficits when compared with the same lesion in the adult. Just as the anatomical consequences of injury to the developing nervous system are not uniform, similarly, the behavioral consequences are also not uniform. Spinal cord injury before the mature pattern of locomotion has developed results in a different motor strategy than after injury in the adult.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  M. Goldberger,et al.  Infant lesion effect: II. Sparing and recovery of function after spinal cord damage in newborn and adult cats. , 1983, Brain research.

[2]  Janet Marie Donatelle.  Growth of the corticospinal tract and the development of placing reactions in the postnatal rat , 1977, The Journal of comparative neurology.

[3]  D. Stelzner,et al.  Anatomical studies of dorsal column axons and dorsal root ganglion cells after spinal cord injury in the newborn rat , 1990, The Journal of comparative neurology.

[4]  K. Kalil,et al.  Functional role of regrowing pyramidal tract fibers , 1982, The Journal of comparative neurology.

[5]  R. Glassman.  Similar effects of infant and adult sensorimotor cortical lesions on cats' posture. , 1973, Brain research.

[6]  M. Murray,et al.  Plasticity of spinal systems after unilateral lumbosacral dorsal rhizotomy in the adult rat , 1991, The Journal of comparative neurology.

[7]  P. Dederen,et al.  An anterograde tracer study of the developing corticospinal tract in the rat: three components. , 1987, Brain research.

[8]  R. Passingham,et al.  Failure to develop a precision grip in monkeys with unilateral neocortical lesions made in infancy , 1978, Brain Research.

[9]  P. Reier,et al.  Neural tissue transplants rescue axotomized rubrospinal cells from retrograde death , 1986, The Journal of comparative neurology.

[10]  M. Goldberger,et al.  Restitution of function and collateral sprouting in the cat spinal cord: The deafferented animal , 1974, The Journal of comparative neurology.

[11]  G. Martin,et al.  Developmental sequence in the origin of descending spinal pathways. Studies using retrograde transport techniques in the North American opossum (Didelphis virginiana). , 1984, Brain research.

[12]  W. Ershler,et al.  Effects of spinal transection in neonatal and weanling rats: Survival of function , 1975, Experimental Neurology.

[13]  D. Stelzner,et al.  The development of descending and dorsal root connections in the lumbosacral spinal cord of the postnatal rat , 1979, The Journal of comparative neurology.

[14]  H Forssberg,et al.  Tactile placing reactions in chronic spinal kittens. , 1974, Acta physiologica Scandinavica.

[15]  I. Whishaw,et al.  Sparing of skilled forelimb reaching and corticospinal projections after neonatal motor cortex removal or hemidecortication in the rat: support for the Kennard doctine , 1988, Brain Research.

[16]  N. Schneiderman,et al.  The intermediolateral nucleus: an ‘open’ or ‘closed’ nucleus? , 1986, Brain Research.

[17]  G. Martin,et al.  Development of catecholaminergic projections to the spinal cord in the North American opossum, Didelphis virginiana , 1990, The Journal of comparative neurology.

[18]  I. Whishaw,et al.  Recovery from early cortical lesions in rats. III. Neonatal removal of posterior parietal cortex has greater behavioral and anatomical effects than similar removals in adulthood , 1987, Behavioural Brain Research.

[19]  R. Coggeshall,et al.  A comparison of axonal numbers in dorsal roots following spinal cord hemisection in neonate and adult rats , 1983, Brain Research.

[20]  S. Grillner,et al.  Some Aspects on the Descending Control of the Spinal Circuits Generating Locomotor Movements , 1976 .

[21]  D. Stelzner,et al.  Ascending tract neurons survive spinal cord transection in the neonatal rat , 1986, Experimental Neurology.

[22]  B. Bregman,et al.  Both regenerating and late-developing pathways contribute to transplant-induced anatomical plasticity after spinal cord lesions at birth , 1991, Experimental Neurology.

[23]  M. Kennard,et al.  RELATION OF AGE TO MOTOR IMPAIRMENT IN MAN AND IN SUBHUMAN PRIMATES , 1940 .

[24]  D. Stelzner,et al.  Changes in the magnocellular portion of the red nucleus following thoracic hemisection in the neonatal and adult rat , 1976, The Journal of comparative neurology.

[25]  B. Bregman.  Development of serotonin immunoreactivity in the rat spinal cord and its plasticity after neonatal spinal cord lesions. , 1987, Brain research.

[26]  M. Kennard.  Age and other factors in motor recovery from precentral lesions in monkeys. , 1936 .

[27]  M. Goldberger,et al.  Infant lesion effect: I. Development of motor behavior following neonatal spinal cord damage in cats. , 1983, Brain research.

[28]  B. Bregman.  Spinal cord transplants permit the growth of serotonergic axons across the site of neonatal spinal cord transection. , 1987, Brain research.

[29]  Amassian Ve,et al.  Developing role of sensorimotor cortex and pyramidal tract neurons in contact placing in kittens. , 1978 .

[30]  D. Stelzner,et al.  A comparison of the effect of mid-thoracic spinal hemisection in the neonatal or weanling rat on the distribution and density of dorsal root axons in the lumbosacral spinal cord of the adult , 1979, Brain Research.

[31]  E. Jones,et al.  Growing corticospinal axons by-pass lesions of neonatal rat spinal cord , 1983, Neuroscience.

[32]  A. Tessler,et al.  Death of some dorsal root ganglion neurons and plasticity of others following sciatic nerve section in adult and neonatal rats , 1989, The Journal of comparative neurology.

[33]  K. Kalil,et al.  Cell death of corticospinal neurons is induced by axotomy before but not after innervation of spinal targets , 1990, The Journal of comparative neurology.

[34]  R. Thompson,et al.  Differential effects of cortical lesions in infant and adult cats on roughness discrimination. , 1959, Experimental neurology.

[35]  B. Stanfield,et al.  The recovery of forelimb-placing behavior in rats with neonatal unilateral cortical damage involves the remaining hemisphere , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  G. Martin,et al.  Evidence for developmental plasticity of the rubrospinal tract. Studies using the North American opossum. , 1988, Brain research.

[37]  M. Murray,et al.  Restitution of function and collateral sprouting in the cat spinal cord: The partially hemisected animal , 1974, The Journal of comparative neurology.

[38]  T. Phillips,et al.  Comparison of the effect of midthoracic spinal hemisection at birth or in adulthood on motor behavior in the adult rat , 1982, Experimental Neurology.

[39]  M. Goldberger,et al.  Patterns of sprouting and implications for recovery of function. , 1988, Advances in neurology.

[40]  B. Bregman,et al.  Extension of the critical period for developmental plasticity of the corticospinal pathway , 1989, The Journal of comparative neurology.

[41]  A. Castro,et al.  Limb preference after unilateral pyramidotomy in adult and neonatal rats , 1980, Physiology & Behavior.

[42]  K. Kalil,et al.  Effects of infant versus adult pyramidal tract lesions on locomotor behavior in hamsters , 1991, Experimental Neurology.

[43]  M. Murray,et al.  Plasticity of dorsal root and descending serotoninergic projections after partial deafferentation of the adult rat spinal cord , 1990, The Journal of comparative neurology.

[44]  M. Goldberger,et al.  Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral lumbosacral dorsal rhizotomy in adult cats , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  W. Chambers,et al.  Intraspinal sprouting of dorsal root axons; development of new collaterals and preterminals following partial denervation of the spinal cord in the cat. , 1958, A.M.A. archives of neurology and psychiatry.

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

[47]  Gerald E. Schneider,et al.  Is it really better to have your brain lesion early? a revision of the “Kennard Principle” , 1979, Neuropsychologia.

[48]  M. Goldberger,et al.  Anatomical plasticity and sparing of function after spinal cord damage in neonatal cats. , 1982, Science.

[49]  T. Carlstedt.  Reinnervation of the mammalian spinal cord after neonatal dorsal root crush , 1988, Journal of neurocytology.

[50]  G. Martin,et al.  Developmental plasticity of the rubrospinal tract in the North American opossum , 1989, The Journal of comparative neurology.

[51]  D. Stelzner,et al.  Behavioral effects of spinal cord transection in the developing rat , 1977, Brain Research.

[52]  D. Tolbert,et al.  Redirected growth of pyramidal tract axons following neonatal pyramidotomy in cats , 1987, The Journal of comparative neurology.

[53]  J. Prendergast,et al.  Sprouting by tracts descending from the midbrain to the spinal cord: The result of thoracic funiculotomy in the newborn, 21-day-old, and adult rat , 1980, Experimental Neurology.

[54]  D. Stelzner,et al.  Plasticity of the corticospinal tract following midthoracic spinal injury in the postnatal rat , 1983, The Journal of comparative neurology.

[55]  R. Isaacson,et al.  Task dependent recovery after early brain damage. , 1973, Behavioral biology.

[56]  M. Goldberger,et al.  Infant lesion effect: III. Anatomical correlates of sparing and recovery of function after spinal cord damage in newborn and adult cats. , 1983, Brain research.

[57]  H. Karten,et al.  Characterization and quantification of peptidergic amacrine cells in the turtle retina: Enkephalin, neurotensin, and glucagon , 1983, The Journal of comparative neurology.

[58]  B. Kolb,et al.  Neonatal motor cortex lesions in the rat: absence of sparing of motor behaviors and impaired spatial learning concurrent with abnormal cerebral morphogenesis. , 1983, Behavioral neuroscience.