Neonatal maternal separation and enhancement of the inspiratory (phrenic) response to hypoxia in adult rats: Disruption of GABAergic neurotransmission in the nucleus tractus solitarius

European Journal of Neuroscience

Volumn 27, Issue 5, 2008, Pages 1174-1188

  Kinkead, Richard ^a   Balon, Norbert ^a   Genest, Sophie Emmanuelle ^a   Gulemetova, Roumiana ^a   Laforest, Sylvie ^a   Drolet, Guy ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Control of breathing; Development; GABA; Hypoxia; Respiration

Indexed keywords

4 AMINOBUTYRIC ACID;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTERIAL GAS; ARTICLE; CARDIOVASCULAR RESPONSE; CONTROLLED STUDY; FEMALE; GABAERGIC TRANSMISSION; HYPOXIA; INSPIRATORY CAPACITY; MATERNAL DEPRIVATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SOLITARY TRACT NUCLEUS;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; FEMALE; GAMMA-AMINOBUTYRIC ACID; INHALATION; MALE; MATERNAL DEPRIVATION; PHRENIC NERVE; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SOLITARY NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 41149150936     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06082.x     Document Type: Article

References (52)

1. Bavis, R.W., Olson, E.B. Jr., Vidruk, E.H., Fuller, D.D. Mitchell, G.S. (2004) Developmental plasticity of the hypoxic ventilatory response in rats induced by neonatal hypoxia. J. Physiol., 557, 645 660.
2. Bowers, G., Cullinan, W.E. Herman, J.P. (1998) Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J. Neurosci., 18, 5938 5947.
3. Caldji, C., Diorio, J., Anisman, H. Meaney, M.J. (2004) Maternal behavior regulates benzodiazepine/GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice. Neuropsychopharmacology, 29, 1344 1352.
4. Caldji, C., Diorio, J. Meaney, M.J. (2000a) Variations in maternal care in infancy regulate the development of stress reactivity. Biol. Psychiatry, 48, 1164 1174.
5. Caldji, C., Francis, D., Sharma, S., Plotsky, P.M. Meaney, M.J. (2000b) The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology, 22, 219.
6. Carroll, J.L. (2003) Plasticity in respiratory motor control: invited review: developmental plasticity in respiratory control. J. Appl. Physiol., 94, 375 389.
7. Feldman, J.L., Mitchell, G.S. Nattie, E.E. (2003) Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci., 26, 239 266.
8. Finley, J.C. Katz, D.M. (1992) The central organization of carotid body afferent projections to the brainstem of the rat. Brain Res., 572, 108 116.
9. Fong, A.Y., Stornetta, R.L., Foley, C.M. Potts, J.T. (2005) Immunohistochemical localization of GAD67-expressing neurons and processes in the rat brainstem: subregional distribution in the nucleus tractus solitarius. J. Comp. Neurol., 493, 274 290.
10. Francis, D.D. Meaney, M.J. (1999) Maternal care and the development of stress responses. Curr. Opin. Neurobiol., 9, 128 134.
11. Fritschy, J.M. Brunig, I. (2003) Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol. Ther., 98, 299 323.
12. Genest, S.E., Balon, N., Gulemetova, R., Laforest, S., Drolet, G. Kinkead, R. (2007a) Neonatal maternal separation and enhancement of the hypoxic ventilatory response: the role of GABAergic neurotransmission within the paraventricular nucleus of the hypothalamus. J. Physiol., 554. 2, 299 314.
13. Genest, S.E., Gulemetova, R., Laforest, S., Drolet, G. Kinkead, R. (2004) Neonatal maternal separation and sex-specific plasticity of the hypoxic ventilatory response in awake rat. J. Physiol., 554, 543 557.
14. Genest, S.E., Gulemetova, R., Laforest, S., Drolet, G. Kinkead, R. (2007b) Neonatal maternal separation induces sex-specific augmentation of the hypercapnic ventilatory response in awake rat. J. Appl. Physiol., 102, 1416 1421.
15. Gonzalez, C., Almaraz, L., Obeso, A. Rigual, R. (1994) Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol. Rev., 74, 829 898.
16. Gunnar, M.R. (2003) Integrating neuroscience and psychological approaches in the study of early experiences. Ann. N Y Acad. Sci., 1008, 238 247.
17. Herman, J.P. Larson, B.R. (2001) Differential regulation of forebrain glutamic acid decarboxylase mRNA expression by aging and stress. Brain Res., 912, 60.
18. Housley, G.D., Martin-Body, R.L., Dawson, N.J. Sinclair, J.D. (1987) Brain stem projections of the glossopharyngeal nerve and its carotid sinus branch in the rat. Neuroscience, 22, 237 250.
19. Housley, G.D. Sinclair, J.D. (1988) Localization by kainic acid lesions of neurones transmitting the carotid chemoreceptor stimulus for respiration in rat. J. Physiol., 406, 99 114.
20. Hsu, F.C., Zhang, G.J., Raol, Y.S., Valentino, R.J., Coulter, D.A. Brooks-Kayal, A.R. (2003) Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses. Proc. Natl Acad. Sci. USA, 100, 12213 12218.
21. Jaworski, J., Francis, D., Brommer, C., Morgan, E. Kuhar, M. (2005) Effects of early maternal separation on ethanol intake, GABA receptors and metabolizing enzymes in adult rats. Psychopharmacology, 181, 8 15.
22. Kara, T., Narkiewicz, K. Somers, V.K. (2003) Chemoreflexes - physiology and clinical implications. Acta Physiol. Scand., 177, 377 384.
23. Kinkead, R., Genest, S.E., Gulemetova, R., Lajeunesse, Y., Laforest, S., Drolet, G. Bairam, A. (2005a) Neonatal maternal separation and early life programming of the hypoxic ventilatory response in rats. Respir. Physiol. Neurobiol., 149, 313 324.
24. Kinkead, R., Gulemetova, R. Bairam, A. (2005b) Neonatal maternal separation enhances phrenic responses to hypoxia and carotid sinus nerve stimulation in the adult anesthetised rat. J. Appl. Physiol., 99, 189 196.
25. 2 receptor and tyrosine hydroxylase mRNA expression levels in carotid body of rats. Can. J. Physiol. Pharmacol., 83, 76 84.
26. de Kloet, E.R., Sibug, R.M., Helmerhorst, F.M. Schmidt, M. (2005) Stress, genes and the mechanism of programming the brain for later life. Neurosci. Biobehav. Rev., 29, 271 281.
27. Kuhn, C.M. Schanberg, S.M. (1998) Responses to maternal separation: mechanisms and mediators. Int. J. Dev. Neurosci., 16, 261 270.
28. Ladd, C.O., Huot, R.L., Thrivikraman, K.V., Nemeroff, C.B., Meaney, M.J. Plotsky, P.M. (2000) Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res., 122, 81 103.
29. Lehmann, J. Feldon, J. (2000) Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing? Rev. Neurosci., 11, 383 408.
30. Levine, S. (2005) Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology, 30, 939 946.
31. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P.M. Meaney, M.J. (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science, 277, 1659 1662.
32. Macri, S. Wurbel, H. (2006) Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Hormones Behav., 50, 667 680.
33. Mansi, J.A., Laforest, S. Drolet, G. (2000) Effect of stress exposure on the activation pattern of enkephalin-containing perikarya in the rat ventral medulla. J. Neurochem., 74, 2568 2575.
34. Marty, S., da, M. Berninger, B. (1997) Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci., 20, 198 202.
35. Mei, L., Zhang, J. Mifflin, S. (2003) Hypertension alters GABA receptor-mediated inhibition of neurons in the nucleus of the solitary tract. Am. J. Physiol. Regul. Integr. Comp. Physiol., 285, R1276 R1286.
36. Mortola, J.P. (2001) Respiratory Physiology of Newborn Mammals: A Comparative Perspective. The Johns Hopkins University Press, Baltimore.
37. Patel, A.B., de Graaf, R.A., Martin, D.L., Battaglioli, G. Behar, K.L. (2006) Evidence that GAD65 mediates increased GABA synthesis during intense neuronal activity in vivo. J. Neurochem., 97, 385 396.
38. Paxinos, G. Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
39. Powell, F.L., Milsom, W.K. Mitchell, G.S. (1998) Time domains of the hypoxic ventilatory response. Respir. Physiol., 112, 123 134.
40. Rimvall, K. Martin, D.L. (1994) The level of GAD67 protein is highly sensitive to small increases in intraneuronal gamma-aminobutyric acid levels. J. Neurochem., 62, 1375 1381.
41. Schousboe, A. Redburn, D.A. (1995) Modulatory actions of gamma aminobutyric acid (GABA) on GABA type A receptor subunit expression and function. J. Neurosci. Res., 41, 1 7.
42. Seckl, J.R. Meaney, M.J. (1993) Early life events and later development of ischaemic heart disease. Lancet, 342, 1236.
43. Sieghart, W. (1995) Structure and pharmacology of gamma-aminobutyric acidA receptor subtypes. Pharmacol. Rev., 47, 181 234.
44. Smith, C.A., Nakayama, H. Dempsey, J.A. (2003) The essential role of carotid body chemoreceptors in sleep apnea. Can. J. Physiol. Pharmacol., 81, 774 779.
45. Smith, M.L. Pacchia, C.F. (2007) Sleep apnoea & hypertension: physiological bases for a causal relation: sleep apnoea and hypertension: role of chemoreflexes in humans. Exp. Physiol., 92, 45 50.
46. Soghomonian, J.J. Martin, D.L. (1998) Two isoforms of glutamate decarboxylase: why? Trends Pharmacol. Sci., 19, 500 505.
47. Swanwick, C.C., Murthy, N.R. Kapur, J. (2006) Activity-dependent scaling of GABAergic synapse strength is regulated by brain-derived neurotrophic factor. Mol. Cell. Neurosci., 31, 481 492.
48. Tabata, M., Kurosawa, H., Kikuchi, Y., Hida, W., Ogawa, H., Okabe, S., Tun, Y., Hattori, T. Shirato, K. (2001) Role of GABA within the nucleus tractus solitarii in the hypoxic ventilatory decline of awake rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 281, R1411 R1419.
49. Tolstykh, G., Belugin, S. Mifflin, S. (2004) Responses to GABAA receptor activation are altered in NTS neurons isolated from chronic hypoxic rats. Brain Res., 1006, 107.
50. Weaver, I.C., Cervoni, N., Champagne, F.A., D'Alessio, A.C., Sharma, S., Seckl, J.R., Dymov, S., Szyf, M. Meaney, M.J. (2004) Epigenetic programming by maternal behavior. Nat. Neurosci., 7, 847 854.
51. Younes, M. (2004) Role of arousals in the pathogenesis of obstructive sleep apnea. Am. J. Respir. Crit. Care Med., 169, 623 633.
52. Younes, M., Ostrowski, M., Thompson, W., Leslie, C. Shewchuk, W. (2001) Chemical control stability in patients with obstructive sleep apnea. Am. J. Respir. Crit. Care Med., 163, 1181 1190.