Postural Modifications and Neuronal Excitability Changes Induced by a Short-Term Serotonin Depletion during Neonatal Development in the Rat

Journal of Neuroscience

Volumn 22, Issue 12, 2002, Pages 5108-5117

  Pflieger, Jean François ^a   Clarac, François ^a   Vinay, Laurent ^a  

^a CNRS   (France)

Author keywords

Development; Motoneurons; Motor behaviors; Posture; Rat; Serotonin; Spinal cord; Spontaneous activity

Indexed keywords

FENCLONINE; SEROTONIN; ENZYME INHIBITOR; TRYPTOPHAN HYDROXYLASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANKLE; ARTICLE; BODY POSTURE; CELL MATURATION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; INTERNEURON; INTRACELLULAR RECORDING; KNEE FUNCTION; MOTOR NERVE CONDUCTION; MUSCLE INNERVATION; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NEWBORN; NONHUMAN; PERINATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SEROTONIN RELEASE; SEROTONINERGIC NERVE CELL; SHAM FEEDING; SPECIES COMPARISON; SPINAL CORD MOTONEURON; ANIMAL; ANIMAL BEHAVIOR; DRUG ANTAGONISM; GROWTH, DEVELOPMENT AND AGING; HIP; HISTOLOGY; KINETICS; KNEE; LUMBAR VERTEBRA; MOTONEURON; MOTOR ACTIVITY; NERVE CONDUCTION; PHYSIOLOGY; SPINAL CORD; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; ANKLE JOINT; BEHAVIOR, ANIMAL; ENZYME INHIBITORS; FENCLONINE; HIP; KINETICS; KNEE; LUMBAR VERTEBRAE; MOTOR ACTIVITY; MOTOR NEURONS; NEURAL CONDUCTION; POSTURE; RATS; RATS, WISTAR; SEROTONIN; SPINAL CORD; TRYPTOPHAN HYDROXYLASE;

EID: 0037096257     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-12-05108.2002     Document Type: Article

References (61)

1. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24:353-360.
2. Berger AJ, Bayliss DA, Viana F (1996) Development of hypoglossal motoneurons. J Appl Physiol 81:1039-1048.
3. Bolles RC, Woods PJ (1964) The ontogeny of behaviour in the albino rat. Anim Behav 12:427-441.
4. Bou-Flores C, Lajard AM, Monteau R, De Maeyer E, Seif I, Lanoir J, Hilaire G (2000) Abnormal phrenic motoneuron activity and morphology in neonatal monoamine oxidase A-deficient transgenic mice: possible role of a serotonin excess. J Neurosci 20:4646-4656.
5. Bregman BS (1987) Development of serotonin immunoreactivity in the rat spinal cord and its plasticity after neonatal spinal cord lesions. Brain Res 431:245-263.
6. Brocard F, Vinay L, Clarac F (1999a) Development of hindlimb postural control during the first postnatal week in the rat. Dev Brain Res 117:81-89.
7. Brocard F, Vinay L, Clarac F (1999b) Gradual development of the ventral funiculus input to lumbar motoneurons in the neonatal rat. Neuroscience 90:1543-1554.
8. Burnet H, Bevengut M, Chakri F, Bou-Flores C, Coulon P, Gaytan S, Pasaro R, Hilaire G (2001) Altered respiratory activity and respiratory regulations in adult monoamine oxidase A-deficient mice. J Neurosci 21:5212-5221.
9. Buznikov GA, Lambert HW, Lauder JM (2001) Serotonin and serotonin-like substances as regulators of early embryogenesis and morphogenesis. Cell Tissue Res 305:177-186.
10. Cameron WE, Nunez-Abades PA, Kerman IA, Hodgson TM (2000) Role of potassium conductances in determining input resistance of developing brain stem motoneurons. J Neurophysiol 84:2330-2339.
11. Cazalets JR, Gardette M, Hilaire G (2000) Locomotor network maturation is transiently delayed in the MAOA-deficient mouse. J Neurophysiol 83:2468-2470.
12. Chang Q, Gonzalez M, Pinter MJ, Balice-Gordon RJ (1999) Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J Neurosci 19:10813-10828.
13. Dekkers J, Becker DL, Cook JE, Navarrete R (1994) Early postnatal changes in the somatodendritic morphology of ankle flexor motoneurons in the rat. Eur J Neurosci 6:87-97.
14. Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, Couraud F, Zalc B, Lubetzki C (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci USA 93:9887-9892.
15. Fellippa-Marques S, Vinay L, Clarac F (2000) Spontaneous and locomotor-related GABAergic input onto primary afferents in the neonatal rat. Eur J Neurosci 12:155-164.
16. Fulton BP, Walton K (1986) Eleetrophysiological properties of neonatal rat motoneurones studied in vitro. J Physiol (Lond) 370:651-678.
17. Gao B-X, Ziskind-Conhaim L (1995) Development of glycine- and GABA-gated currents in rat spinal motoneurons. J Neurophysiol 74:113-121.
18. Gao BX, Ziskind-Conhaim L (1998) Development of ionic currents underlying changes in action potential waveforms in rat spinal motoneurons. J Neurophysiol 80:3047-3061.
19. Geisler HC, Westerga J, Gramsbergen A (1993) Development of posture in the rat. Acta Neurobiol Exp (Wars) 53:517-523.
20. Haydon PG, McCobb DP, Kater SB (1984) Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons. Science 226:561-564.
21. Jacobs BL, Fornal CA (1993) 5-HT and motor control: a hypothesis. Trends Neurosci 16:346-352.
22. Jakowec MW, Fox AJ, Martin LJ, Kalb RG (1995) Quantitative and qualitative changes in AMPA receptor expression during spinal cord development. Neuroscience 67:893-907.
23. Jankowska E, Hammar I, Chojnicka B, Heden CH (2000) Effects of monoamines on interneurons in four spinal reflex pathways from group I and/or group II muscle afferents. Eur J Neurosci 12:701-714.
24. Kalb RG, Lidow MS, Halsted MJ, Hockfield S (1992) N-methyl-D-aspartate receptors are transiently expressed in the developing spinal cord ventral horn. Proc Natl Acad Sci USA 89:8502-8506.
25. Kerai B, Greensmith L, Vrbova G, Navarrete R (1995) Effect of transient neonatal muscle paralysis on the growth of soleus motoneurones in the rat. Dev Brain Res 85:89-95.
26. Kiehn O, Erdal J, Eken T, Bruhn T (1996) Selective depletion of spinal monoamines changes the rat soleus EMG from a tonic to a more phasic pattern. J Physiol (Lond) 492:173-184.
27. Koe BK, Weissman A (1966) p-Chlorophenylalanine: a specific depletor of brain serotonin. J Pharmacol Exp Ther 154:499-516.
28. Kojima T, Homma S, Sako H, Shimizu I, Okada A, Okado N (1988) Developmental changes in density and distribution of serotoninergic fibers in the chick spinal cord. J Comp Neurol 267:580-589.
29. Kudo N, Furukawa F, Okado N (1993) Development of descending fibers to the rat embryonic spinal cord. Neurosci Res 16:131-141.
30. Lakke EAJF (1997) The projections to the spinal cord of the rat during development: a time-table of descent. Adv Anat Embryol Cell Biol 135:1-143.
31. Lauder JM (1993) Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 16:233-240.
32. Mazer C, Muneyyirci J, Taheny K, Raio N, Borella A, Whitaker-Azmitia P (1997) Serotonin depletion during synaptogenesis leads to decreased synaptic density and learning deficits in the adult rat: a possible model of neurodevelopmental disorders with cognitive deficits. Brain Res 760:68-73.
33. Myoga H, Nonaka S, Matsuyama K, Mori S (1995) Postnatal development of locomotor movements in normal and parachlorophenylalanine-treated newborn rats. Neurosci Res 21:211-221.
34. Nakajima K, Matsuyama K, Mori F (1996) Prenatal suppression of serotonergic system results in movement disorders and hypoplesia of extensor motoneurons in newborn rats. Soc Neurosci Abstr 22:1228.
35. Nakajima K, Matsuyama K, Mori S (1998) Prenatal administration of para-chlorophenylalanine results in suppression of serotonergic system and disturbance of swimming movements in newborn rats. Neurosci Res 31:155-169.
36. Nakayama K, Nishimaru H, Iizuka M, Ozaki S, Kudo N (1999) Rostrocaudal progression in the development of periodic spontaneous activity in fetal rat spinal motor circuits in vitro. J Neurophysiol 81:2592-2595.
37. Narayanan CH, Fox MW, Hamburger V (1971) Prenatal development of spontaneous and evoked activity in the rat (Rattus Norvegicus Albinus). Behaviour 40:100-135.
38. Navarrete R, Vrbova G (1993) Activity-dependent interactions between motoneurones and muscles: their role in the development of the motor unit. Prog Neurobiol 41:93-124.
39. Nicolopoulos-Stournaras S, Iles JF (1983) Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217:75-85.
40. Nishimaru H, Iizuka M, Ozaki S, Kudo N (1996) Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. J Physiol (Lond) 497:131-143.
41. Nunez-Abades PA, Pattillo JM, Hodgson TM, Cameron WE (2000) Role of synaptic inputs in determining input resistance of developing brain stem motoneurons. J Neurophysiol 84:2317-2329.
42. O'Donovan MJ (1999) The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol 9:94-104.
43. Okado N, Homma S, Ishihara R, Sako H, Kohno K (1988) Differential innervation of specific motor neuron pools by serotoninergic fibers in the chick spinal cord. Neurosci Lett 94:29-32.
44. Okado N, Cheng L, Tanatsugu Y, Hamada S, Hamaguchi K (1993) Synaptic loss following removal of serotoninergic fibers in newly hatched and adult chickens. J Neurobiol 24:687-698.
45. Pflieger J-F, Clarac F, Vinay L (2000) Effects of serotonin depletion on the maturation of ankle flexor and extensor motoneurons in neonatal rats. Soc Neurosci Abstr 26:257.5.
46. Rajaofetra N, Sandillon F, Geffard M, Privat A (1989) Pre- and postnatal ontogeny of serotonergic projections to the rat spinal cord. J Neurosci Res 22:305-321.
47. Rörig B, Sutor B (1996) Serotonin regulates gap junction coupling in the developing rat somatosensory cortex. Eur J Neurosci 8:1685-1695.
48. Schmidt BJ, Jordan LM (2000) The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53:689-710.
49. Seebach BS, Mendell LM (1996) Maturation in properties of motoneurons and their segmental input in the neonatal rat. J Neurophysiol 76:3875-3885.
50. Sillar KT, Woolston AM, Wedderburn JF (1995) Involvement of brainstem serotonergic interneurons in the development of a vertebrate spinal locomotor circuit. Proc R Soc Lond B Biol Sci 259:65-70.
51. Steinbusch HW (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557-618.
52. Stevens B, Tanner S, Fields RD (1998) Control of myelination by specific patterns of neural impulses. J Neurosci 18:9303-9311.
53. Sullivan JM, Benton JL, Beltz BS (2000) Serotonin depletion in vivo inhibits the branching of olfactory projection neurons in the lobster deutocerebrum. J Neurosci 20:7716-7721.
54. Tanaka H, Mori S, Kimura H (1992) Developmental changes in the serotoninergic innervation of hindlimb extensor motoneurons in neonatal rats. Dev Brain Res 65:1-12.
55. Tohyama I, Kameyama M, Kimura H (1988) Quantitative morphometric analysis of two types of serotonin-immunoreactive nerve fibres differentially responding to p-chlorophenylalanine treatment in the rat brain. Neuroscience 26:971-991.
56. Vinay L, Brocard F, Clarac F (2000a) Differential maturation of motoneurons innervating ankle flexor and extensor muscles in the neonatal rat. Eur J Neurosci 12:4562-4566.
57. Vinay L, Brocard F, Pflieger J, Simeoni-Alias J, Clarac F (2000b) Perinatal development of lumbar motoneurons and their inputs in the rat. Brain Res Bull 53:635-647.
58. Walton K, Navarrete R (1991) Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. J Physiol (Lond) 433:283-305.
59. Westerga J, Gramsbergen A (1992) Structural changes of the soleus and the tibialis anterior motoneuron pool during development in the rat. J Comp Neurol 319:406-416.
60. Wu W-L, Ziskind-Conhaim L, Sweet MA (1992) Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12:3935-3945.
61. Ziskind-Conhaim L (1988) Physiological and morphological changes in developing peripheral nerves of rat embryos. Dev Brain Res 42:15-28.