Advertisement

Development of Interlimb Coordination in the Neonatal Rat

  • Francois Clarac
  • Edouard Pearlstein
  • Jean François Pflieger
  • Laurent Vinay

Abstract

Locomotion is a type of motor behaviour that is produced by spinal neuronal networks associated with the different limbs. The rat in which development lasts three weeks in utero and continues during the first three post-natal weeks appears to be a very attractive model for the study of interlimb coordination maturational mechanisms. An early expression of rhythmic locomotor activity is observed at birth in vitro. Neuroactive substances like excitatory amino acid or amines (5-HT...) applied on the entire brainstem/spinal cord preparation induce a unique rhythmical activity over the cervical and the lumbar generators. This strict coordination results from a mutual interaction between generators since both bursting frequencies are altered significantly after functional isolation, with a slowing down of the isolated cervical network and a significant acceleration of the lumbar burst generator. However the rat does not walk at birth due to an absence of postural regulations. During the first two weeks, the neonatal rat is able to swim or to produce “air stepping” with an ipsilateral and a contralateral alternation between the different limbs. Adult walking occurs only during the third postnatal week. At least two mechanisms are able to control this early interlimb coordination . Numerous studies showed that 5-HT has ubiquitous topic and trophic effects on the early development of neurons and synapses. Studies on “PCPA” treated and “spinal” neonatal rats demonstrated strong deficits in locomotor movements. The second mechanism concerns the sensory afferents after birth; proprioceptive peripheral loops feed the central network and adapt its activation in a coordinated manner.

Key words

Central Pattern Generator (CPG) gait in vitro preparation proprioceptive control serotonin (5-HT) 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ballion B, Morin D, Viala D. (2001) Forelimb locomotor generators and quadrupedal locomotion in the neonatal rat. Eur J Neurosci 14:1727-1738PubMedCrossRefGoogle Scholar
  2. Ben Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728-739PubMedCrossRefGoogle Scholar
  3. Brocard F, Vinay L, Clarac F (l999a) Development of hind-limb postural control during the first post-natal week in the rat. Brain Res Dev Brain Res 117:81-89PubMedCrossRefGoogle Scholar
  4. Brocard F, Vinay L, Clarac F (1999b) Gradual development of the ventral funiculus’s input to lumbar motoneurons in the neonatal rat. Neuroscience 90:1543-1554PubMedCrossRefGoogle Scholar
  5. Brunjes PC, Frazier LL (1986) Maturation and plasticity in the olfactory system of vertebrates. Brain Res 396:1-45PubMedCrossRefGoogle Scholar
  6. Butt STB, Harris-Warrick RH, Kiehn O (2002) Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J Neurosci 22(22):99619971PubMedGoogle Scholar
  7. Cazalets JR, Menard I, Cremieux J, Clarac F (1990) Variability as a characteristic of immature motor systems : an electromyographic study of swimming in the newborn rat. Behav Brain Res 40:215-225PubMedCrossRefGoogle Scholar
  8. Cazalets JR, Sqalli-Houssaini Y, Clarac F (1992) Activation of the central pattern generators for locomotion by serotonin and excitatory amino-acids in neonatal rats. J Physiol (London) 455:187-204Google Scholar
  9. Cazalets JR, Borde M, Clarac F (1995) Localisation and organization of the central pattern generator for hindlimb locomotion in newborn rat. J Neurosci 15:4943-4951PubMedGoogle Scholar
  10. Cazalets JR, Bertrand S (2000) Coupling between lumbar and sacral motor networks in the neonatal rat spinal cord. Eur J Neurosci 12:2993-3002PubMedCrossRefGoogle Scholar
  11. Cazalets JR, Gardette M, Hilaire G (2000) Locomotor network maturation is transiently delayed in the MAOA deficient mouse. J Neurophysiol 83:2468-2470PubMedGoogle Scholar
  12. Cazalets JR (2000) Development of the neural correlates of locomotion in rats. In: Kalverboer AF, Gramsbergen A (eds) Handbook of Brain and Behaviour in human development, Kluwer Academic Publishers, Printed in Great Britain, pp. 447-466Google Scholar
  13. Clarac F, Vinay L, Cazalets JR, Fady JC, Jamon M (1998) Role of gravity in the development of posture and locomotion in the neonatal rat. Brain Res Brain Res Rev 28:35-43PubMedCrossRefGoogle Scholar
  14. Clarac F, Brocard F, Pflieger JF, Vinay L (2001) Maturation of locomotion in the neonate rat, comparisons with another higher vertebrate. In: Gantchev N (Ed.), “From basic motor control to functional recovery II”, Bulgarian Academy of Science, Sofia.Google Scholar
  15. Eide AL, Glover J, Kjaerulff O, Kiehn O (1999) Characterization of commissural interneurons in the lumbar region of the neonatal rat spinal cord. J Comp Neurol 403:332-345PubMedCrossRefGoogle Scholar
  16. Fady JC, Jamon M, Clarac F (1998) Early olfactory-induced rhythmic limb activity in the newborn rat. Brain Res Dev Brain Res 108:111-123PubMedCrossRefGoogle Scholar
  17. Gramsbergen A (2001) Neuro-ontogeny of motor behaviour in the rat. In: Kalberboer AF, Gramsbergen A (eds), Handbook of Brain and Behaviour in human development, Kluwer Academic Publishers, pp. 467-512Google Scholar
  18. Gruner JA, Altman J (1980) Swimming in the rat : analysis of locomotor performance in comparison to stepping. Exp Brain Res 40:374-382PubMedGoogle Scholar
  19. Hilaire G, Duron B (1999) Maturation of the mammalian respiratory system. Physiol Rev 79:325-360PubMedGoogle Scholar
  20. Iikuza M, Nishimaru H, Kudo N (1998) Development of the spatial pattern of 5-HT induced locomotor rhythm in the lumbar spinal cord of rat fetuses in vitro. Neurosci Res 31:107-111CrossRefGoogle Scholar
  21. Iles JF, Coles SK (1991) Effects of loading on muscle activity during locomotion in the rat. In: Armstrong OM, Bush BMH (eds), Locomotor neural mechanisms in arthropods and vertebrates, Manchester University Press, Manchester and New York, pp. 196-201Google Scholar
  22. Jamon M, Clarac F (1998). Early walking in the neonatal rat : a kinematic study. Behav Neurosci 112:1218-1228PubMedCrossRefGoogle Scholar
  23. Jensen JL, Schneider K, Ulrich BD, Zernicke RF, Thelen E (1994) Adaptive dynamics of the leg movement patterns of human infants: I. The effects of posture on spontaneous kicking. J Mot Behav 26:303-312CrossRefGoogle Scholar
  24. Kiehn O, Kjaerulff O (1996) Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J Neurophysiol 75:1471-1482Google Scholar
  25. Kjaerulff O, Kiehn O (1997) Crossed rhythmic synaptic input to motoneurons during selective activation ofthe contralateral spinal locomotor network. J Neurosci 17:9433-9447PubMedGoogle Scholar
  26. Kudo N, Yamada T (1985) Development of the monosynaptic stretch reflex in the rat : an in vitro study. J Physiol (London) 369:127-144Google Scholar
  27. Kudo N, Yamada T (1987) Morphological and physiological studies of development of the monosynaptic reflex pathway in the rat lumbar spinal cord. J Physiol (London) 389:441-459Google Scholar
  28. Lev-Tov A, Delvolve I, Kremer E (2000) Sacrocaudal afferents induce rhythmic efferent bursting in isolated spinal cord of neonatal rats. J Neurophysiol 83:888-894PubMedGoogle Scholar
  29. Marchetti C, Beato M, Nistri A (200 I) Alternating rhythmic activity induced by dorsal root stimulation in the neonatal rat spinal cord in vitro. J Physiol (London) 530:105-112CrossRefGoogle Scholar
  30. McEwen ML, Van Hartesveldt C, Stehouwer OJ (1997a) L-Dopa and Quipazine elicit air stepping in neonatal rats with spinal cord transection. Behav Neurosci 111:825-833PubMedCrossRefGoogle Scholar
  31. McEwen ML, Van Hartesveldt C, Stehouwer OJ (1997b) A kinematic comparison ofL-Dopainduced air-stepping and swimming in developing rats. Dev Psychobiol 30:313-327PubMedCrossRefGoogle Scholar
  32. Morin O, Viala O (2002) Coordination of locomotor and respiratory rhythms in vitro are critically dependent on hindlimb sensory inputs. J Neurosci 22:4756-4765PubMedGoogle Scholar
  33. Myoga H, Nonaka S, Matsuyama K, Mori S (1998) Prenatal development of locomotor movement in normal and parachlorophenylalanine-treated newborn rat. Neurosci Res 21:211-221CrossRefGoogle Scholar
  34. Nakajima K, Matsuyama K, Mori S (1998) Prenatal administration of parachlorophenylalanine results in suppression of serotonergic system and disturbance of swimming movement in newborn rats. Neurosci Res 31:155-169PubMedCrossRefGoogle Scholar
  35. Nakajima K, Nishimaru H, Kudo N (2002) Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci 22:10388-10398Google Scholar
  36. Nicolopoulos-Stournaras S, Iles JF (1984) Hindlimb muscle activity during locomotion in the rat (Rattus norvegicus) (Rodentia-Muridea). J Zool Lond 203:427-440CrossRefGoogle Scholar
  37. Norreel JC, Pflieger JF, Pearlstein E, Simeoni-Alias J, Clarac F, Vinay L (2003) Reversible disorganization of the locomotor pattern after neonatal spinal cord transection in the rat. J Neurosci 23:1924-1932PubMedGoogle Scholar
  38. Orlovsky ON, Deliagina TO, Grillner S (1999) Neuronal control of locomotion - from mollusc to man. Oxford University Press, Oxford.CrossRefGoogle Scholar
  39. Pflieger JF, Clarac F, Vinay L (2002) Postural modifications and neuronal excitability changes induced by short-term serotonin depletion during neonatal development in the rat. J Neurosci 22:5108-5117PubMedGoogle Scholar
  40. Smith JC, Feldman JL (1987) In vitro brainstem-spinal cord preparations for study of motor systems for mammalian respiration and locomotion. J Neurosci Methods 21:321-333PubMedCrossRefGoogle Scholar
  41. Sqalli-Houssaini Y, Cazalets JR, Clarac F (1993) Oscillatory propertiesof the central pattern generatorfor locomotion in neonatal rats. J Neurophysiol 70:803-813PubMedGoogle Scholar
  42. Sqalli-Houssaini Y, Cazalets JR (2000) Noradrenergic controlof locomotornetworks in the in vitro spinal cord of the neonatal rat. Brain Res 852:100-109PubMedCrossRefGoogle Scholar
  43. Stehouwer OJ, Van Hartesvedlt C (2000) Kinematic analysis of air stepping in normal and decerebrate preweanling rats. Dev Psychobiol 36:1-8PubMedCrossRefGoogle Scholar
  44. Tanaka H, Mori S, KimuraH (1992) Development changes in the serotoninergic innervation of hindlimbextensormotoneurons in neonatal rats. Dev Brain Res 65:1-12CrossRefGoogle Scholar
  45. Tucker LB, Stehouwer OJ (2000) L-Dopa-induced air stepping in the preweanling rat : electromyographic and kinematic analyses. Behav Neurosci 114:1174-1182PubMedCrossRefGoogle Scholar
  46. Vanderwolf CH, Kolb B, Cooley RK (1978) Behavior of the rat after removal of the neocortex and hippocampal formation. J. Comp Physiol Psychol 92:156-l75PubMedCrossRefGoogle Scholar
  47. Vinay L, Brocard F, Clarac F (2000a) Differential maturation of motoneurons innervating ankle flexorand extensormusclesin the neonatal rat. Eur J of Neurosci 12:4562-4566CrossRefGoogle Scholar
  48. Vinay L, Brocard F, Pflieger JF, Simeoni-Alias J, Clarac F (2000b) Perinatal development of lumbarmotoneurons and their inputs in the rat. Brain Res Bull 53:635-648PubMedCrossRefGoogle Scholar
  49. Von Holst E (1943) Uber relative koordination bei arthropoden. Arch Ges Physiol Pfluger’s 146:846-865Google Scholar

Copyright information

© Springer Science+Business Media New York 2004

Authors and Affiliations

  • Francois Clarac
    • 1
  • Edouard Pearlstein
    • 1
  • Jean François Pflieger
    • 1
  • Laurent Vinay
    • 1
  1. 1.INPCCNRSMarseilleFrance

Personalised recommendations