Ontogenic changes of the GABAergic system in the embryonic mouse spinal cord

Brain Research

Volumn 1000, Issue 1-2, 2004, Pages 134-147

  Allain, Anne Emilie ^a   Baïri, Alexia ^a   Meyrand, Pierre ^a   Branchereau, Pascal ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Development; Development and regeneration; GABA; Immunohistochemistry; Mouse embryo; Pattern formation, compartments and boundaries

Indexed keywords

4 AMINOBUTYRIC ACID;

ANIMAL CELL; ARTICLE; BRACHIAL PLEXUS; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; GABAERGIC SYSTEM; GRAY MATTER; IMMUNOCOMPETENT CELL; LUMBAR SPINE; MOTONEURON; MOUSE; NEWBORN; NONHUMAN; ONTOGENY; PERIKARYON; PRIORITY JOURNAL; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD VENTRAL HORN; WHITE MATTER;

ANIMALS; ANIMALS, NEWBORN; FEMALE; GAMMA-AMINOBUTYRIC ACID; MICE; PREGNANCY; SPINAL CORD;

EID: 1842453270     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2003.11.071     Document Type: Article

References (57)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 94:1946;239-247.
2. Antal M., Berki A.C., Horvath L., O'Donovan M.J. Developmental changes in the distribution of gamma-aminobutyric acid-immunoreactive neurons in the embryonic chick lumbosacral spinal cord. J. Comp. Neurol. 343:1994;228-236.
3. Aoki E., Semba R., Kashiwamata S. When does GABA-like immunoreactivity appear in the rat cerebellar GABAergic neurons? Brain Res. 502:1989;245-251.
4. Ballion B., Branchereau P., Chapron J., Viala D. Ontogeny of descending serotonergic innervation and evidence for intraspinal 5-HT neurons in the mouse spinal cord. Dev. Brain Res. 137:2002;81-88.
5. Behar T.N., Schaffner A.E., Colton C.A., Somogyi R., Olah Z., Lehel C., Barker J.L. GABA-induced chemokinesis and NGF-induced chemotaxis of embryonic spinal cord neurons. J. Neurosci. 14:1994;29-38.
6. Behar T.N., Schaffner A.E., Tran H.T., Barker J.L. GABA-induced motility of spinal neuroblasts develops along a ventrodorsal gradient and can be mimicked by agonists of GABAA and GABAB receptors. J. Neurosci. Res. 42:1995;97-108.
7. Ben-Ari Y. Developing networks play a similar melody. TINS. 24:2001;353-360.
8. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev., Neurosci. 3:2002;728-739.
9. Berki A.C., O'Donovan M.J., Antal M. Developmental expression of glycine immunoreactivity and its colocalization with GABA in the embryonic chick lumbosacral spinal cord. J. Comp. Neurol. 362:1995;583-596.
10. Binor E., Heathcote R.D. Development of GABA-immunoreactive neuron patterning in the spinal cord. J. Comp. Neurol. 438:2001;1-11.
11. Bonnot A., Whelan P.J., Mentis G.Z., O'Donovan M.J. Locomotor-like activity generated by the neonatal mouse spinal cord. Brain Res. Rev. 40:2002;141-151.
12. Borday V., Fortin G., Champagnat J. Early ontogeny of rhythm generation and control of breathing. Respir. Physiol. 110:1997;245-249.
13. Bou-Flores C., Berger A.J. Gap junctions and inhibitory synapses modulate inspiratory motoneuron synchronization. J. Neurophysiol. 85:2001;1543-1551.
14. Branchereau P., Morin D., Bonnot A., Ballion B., Chapron J., Viala D. Development of lumbar rhythmic networks: from embryonic to neonate locomotor-like patterns in the mouse. Brain Res. Bull. 53:2000;711-718.
15. Branchereau P., Chapron J., Meyrand P. Descending 5-hydroxytryptamine raphe inputs repress the expression of serotonergic neurons and slow the maturation of inhibitory systems in mouse embryonic spinal cord. J. Neurosci. 22:2002;2598-2606.
16. Chen G., Trombley P.Q., van den Pol A.N. Excitatory actions of GABA in developing rat hypothalamic neurones. J. Physiol. (Lond.). 494:1996;451-464.
17. Chronwall B., Wolff J.R. Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of rat. J. Comp. Neurol. 190:1980;187-208.
18. Cobas A., Fairen A., Alvarez-Bolado G., Sanchez M.P. Prenatal development of the intrinsic neurons of the rat neocortex: a comparative study of the distribution of GABA-immunoreactive cells and the GABAA receptor. Neuroscience. 40:1991;375-397.
19. Code R.A., Burd G.D., Rubel E.W. Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J. Comp. Neurol. 284:1989;504-518.
20. Coggeshall R.E., Lekan H.A. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J. Comp. Neurol. 364:1996;6-15.
21. Del Rio J.A., Soriano E., Ferrer I. Development of GABA-immunoreactivity in the neocortex of the mouse. J. Comp. Neurol. 326:1992;501-526.
22. Dzhala V.I., Staley K.J. Excitatory actions of endogenously released GABA contribute to initiation of ictal epileptiform activity in the developing hippocampus. J. Neurosci. 23:2003;1840-1846.
23. Ericson J., Thor S., Edlund T., Jessell T.M., Yamada T. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science. 256:1992;1555-1560.
24. Ganguly K., Schinder A.F., Wong S.T., Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell. 105:2001;521-532.
25. Gao B.X., Stricker C., Ziskind-Conhaim L. Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J. Neurophysiol. 86:2001;492-502.
26. Hedreen J.C. Lost caps in histological counting methods. Anat. Rec. 250:1998;366-372.
27. Hokfelt T., Arvidsson U., Cullheim S., Millhorn D., Nicholas A.P., Pieribone V., Seroogy K., Ulfhake B. Multiple messengers in descending serotonin neurons: localization and functional implications. J. Chem. Neuroanat. 18:2000;75-86.
28. Jiang Z., Carlin K.P., Brownstone R.M. An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks. Brain Res. 816:1999;493-499.
29. Jong Y.J., Thampy K.G., Barnes E.M. Jr. Ontogeny of GABAergic neurons in chick brain: studies in vivo and in vitro. Brain Res. 390:1986;83-90.
30. Katarova Z., Sekerkova G., Prodan S., Mugnaini E., Szabo G. Domain-restricted expression of two glutamic acid decarboxylase genes in midgestation mouse embryos. J. Comp. Neurol. 424:2000;607-627.
31. Kullmann P.H., Ene F.A., Kandler K. Glycinergic and GABAergic calcium responses in the developing lateral superior olive. Eur. J. Neurosci. 15:2002;1093-1104.
32. Lauder J.M., Han V.K., Henderson P., Verdoorn T., Towle A.C. Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience. 19:1986;465-493.
33. Lauder J.M., Liu J., Devaud L., Morrow A.L. GABA as a trophic factor for developing monoamine neurons. Perspect. Dev. Neurobiol. 5:1998;247-259.
34. Lawson S.J., Davies H.J., Bennett J.P., Lowrie M.B. Evidence that spinal interneurons undergo programmed cell death postnatally in the rat. Eur. J. Neurosci. 9:1997;794-799.
35. Leinekugel X., Khalilov I., McLean H., Caillard O., Gaiarsa J.L., Ben-Ari Y., Khazipov R. GABA is the principal fast-acting excitatory transmitter in the neonatal brain. Adv. Neurol. 79:1999;189-201.
36. Lev-Tov A., Delvolve I. Pattern generation in non-limb moving segments of the mammalian spinal cord. Brain Res. Bull. 53:2000;671-675.
37. Liu J., Morrow A.L., Devaud L., Grayson D.R., Lauder J.M. GABAA receptors mediate trophic effects of GABA on embryonic brainstem monoamine neurons in vitro. J. Neurosci. 17:1997;2420-2428.
38. Lundgren P., Mattsson M.O., Johansson L., Ottersen O.P., Sellstrom A. Morphological and GABA-immunoreactive development of the embryonic chick telencephalon. Int. J. Dev. Neurosci. 13:1995;463-472.
39. Ma W., Behar T., Barker J.L. Transient expression of GABA immunoreactivity in the developing rat spinal cord. J. Comp. Neurol. 325:1992;271-290.
40. Marty S., Berninger B., Carroll P., Thoenen H. GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron. 16:1996;565-570.
41. Nakayama K., Nishimaru H., Kudo N. Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J. Neurosci. 22:2002;10388-10398.
42. Owens D.F., Kriegstein A.R. Is there more to GABA than synaptic inhibition? Nat. Rev., Neurosci. 3:2002;715-727.
43. Owens D.F., Boyce L.H., Davis M.B., Kriegstein A.R. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16:1996;6414-6423.
44. Peduzzi J.D. Genesis of GABA-immunoreactive neurons in the ferret visual cortex. J. Neurosci. 8:1988;920-931.
45. Phelps P.E., Alijani A., Tran T.S. Ventrally located commissural neurons express the GABAergic phenotype in developing rat spinal cord. J. Comp. Neurol. 409:1999;285-298.
46. Ritter B., Zhang W. Early postnatal maturation of GABAA-mediated inhibition in the brainstem respiratory rhythm-generating network of the mouse. Eur. J. Neurosci. 12:2000;2975-2984.
47. Rozenberg F., Robain O., Jardin L., Ben-Ari Y. Distribution of GABAergic neurons in late fetal and early postnatal rat hippocampus. Dev. Brain Res. 50:1989;177-187.
48. Schwartz M.L., Meinecke D.L. Early expression of GABA-containing neurons in the prefrontal and visual cortices of rhesus monkeys. Cereb. Cortex. 2:1992;16-37.
49. Sernagor E., Grzywacz N.M. Spontaneous activity in developing turtle retinal ganglion cells: pharmacological studies. J. Neurosci. 19:1999;3874-3887.
50. Sernagor E., Young C., Eglen S.J. Developmental modulation of retinal wave dynamics: shedding light on the GABA saga. J. Neurosci. 23:2003;7621-7629.
51. Tran T.S., Phelps P.E. Axons crossing in the ventral commissure express L1 and GAD65 in the developing rat spinal cord. Dev. Neurosci. 22:2000;228-236.
52. Tran T.S., Alijani A., Phelps P.E. Unique developmental patterns of GABAergic neurons in rat spinal cord. J. Comp. Neurol. 456:2003;112-126.
53. Van Eden C.G., Mrzljak L., Voorn P., Uylings H.B. Prenatal development of GABA-ergic neurons in the neocortex of the rat. J. Comp. Neurol. 289:1989;213-227.
54. White A.M., Platt B. Gamma-aminobutyric acid-induced calcium signalling in rat superior collicular neurones. Neurosci. Lett. 334:2002;79-82.
55. Wu W.L., Ziskind-Conhaim L., Sweet M.A. Early development of glycine- and GABA-mediated synapses in rat spinal cord. J. Neurosci. 12:1992;3935-3945.
56. Yamashita A., Hayashi M. Ontogeny of GABA-immunoreactive cells in the primate cerebellar cortex: comparison with somatostatin-immunoreactivity. Anat. Embryol. 194:1996;215-222.
57. Ziskind-Conhaim L. Physiological functions of GABA-induced depolarizations in the developing rat spinal cord. Perspect. Dev. Neurobiol. 5:1998;279-287.