Neonatal maternal separation and enhancement of the hypoxic ventilatory response in rat: The role of GABAergic modulation within the paraventricular nucleus of the hypothalamus

Journal of Physiology

Volumn 583, Issue 1, 2007, Pages 299-314

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

^a LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE; MUSCIMOL; OXYGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BINDING SITE; CONTROLLED STUDY; DISEASE PREDISPOSITION; EXCITATION; GABAERGIC SYSTEM; HOMEOSTASIS; HYPOXIA; LUNG MINUTE VOLUME; MALE; MICROINJECTION; MOTHER CHILD RELATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; RESPIRATION CONTROL; RESPIRATORY TRACT DISEASE; THALAMUS MIDLINE NUCLEUS; BODY TEMPERATURE; GABAERGIC TRANSMISSION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOXIC VENTILATORY RESPONSE; LUNG VENTILATION; MATERNAL DEPRIVATION; NEUROANATOMY;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; ANXIETY, SEPARATION; FEMALE; FLUNITRAZEPAM; GABA AGONISTS; GABA MODULATORS; GAMMA-AMINOBUTYRIC ACID; MALE; MUSCIMOL; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PULMONARY VENTILATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RESPIRATORY MECHANICS; SYNAPTIC TRANSMISSION;

EID: 34547840332     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2007.135160     Document Type: Article

References (59)

1. Anisman H, Zaharia MD, Meaney MJ & Merali Z (1998). Do early-life events permanently alter behavioral and hormonal responses to stressors? Int J Dev Neurosci 16, 149-164.
2. A, NMDA and AMPA receptors: A developmentally regulated 'menage a trois'. Trends Neurosci 20, 523-529.
3. Berquin P, Bodineau L, Gros F & Larnicol N (2000). Brainstem and hypothalamic areas involved in respiratory chemoreflexes: A Fos study in adult rats. Brain Res 857, 30-40.
4. Boudaba C, Szabo K & Tasker JG (1996). Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci 16, 7151-7160.
5. A and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22, 219.
6. B2 subunits in rat brain, spinal cord and dorsal root ganglion. Neuroscience 106, 447-467.
7. Cole RL & Sawchenko PE (2002). Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J Neurosci 22, 959-969.
8. Drolet G, Chalmers J & Blessing W (1993). Vasodepressor neurons in medulla alter cardiac contractility and cardiac output. Hypertension 21, 210-215.
9. Chen X-Q, Du J-Z & Wang YS (2004). Regulation of hypoxia-induced release of corticotropin-releasing factor in the rat hypothalamus by norepinephrine. Regul Pept 119, 221-228.
10. Erickson JT & Millhorn DE (1994). Hypoxia and electrical stimulation of the carotid sinus nerve induce Fos-like immunoreactivity within catecholaminergic and serotoninergic neurons of the rat brainstem. J Comp Neurol 348, 161-182.
11. Finley JC & Katz DM (1992). The central organization of carotid body afferent projections to the brainstem of the rat. Brain Res 572, 108-116.
12. Fournier S, Allard M, Gulemetova R & Kinkead R (2006). Chronic elevation of corticosterone increases the ventilatory response to hypoxia in adult rats. FASEB J 20, A374
13. Genest SE, 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 SE, Gulemetova R, Laforest S, Drolet G & Kinkead R (2007). Neonatal maternal separation induces sex-specific augmentation of the hypercapnic ventilatory response in awake rat. J Appl Physiol 102, 1416-1421.
15. Haywood JR, Mifflin SW, Craig T, Calderon A, Hensler JG & Hinojosa-Laborde C (2001). γ-Aminobutyric acid (GABA) -a function and binding in the paraventricular nucleus of the hypothalamus in chronic renal-wrap hypertension. Hypertension 37, 614-618.
16. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC & Cullinan WE (2003). Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24, 151-180.
17. Herman JP, Tasker JG, Ziegler DR & Cullinan WE (2002). Local circuit regulation of paraventricular nucleus stress integration: Glutamate-GABA connections. Pharmacol Biochem Behav 71, 457-468.
18. Hirooka Y, Polson JW, Potts PD & Dampney RA (1997). Hypoxia-induced Fos expression in neurons projecting to the pressor region in the rostral ventrolateral medulla. Neuroscience 80, 1209-1224.
19. Horn EM, Kramer JM & Waldrop TG (2000). Development of hypoxia-induced Fos expression in rat caudal hypothalamic neurons. Neuroscience 99, 711-720.
20. Housley GD & Sinclair JD (1988). Localization by kainic acid lesions of neurones transmitting the carotid chemoreceptor stimulus for respiration in rat. J Physiol 406, 99-114.
21. A receptor desensitization kinetics and its role in synapse function in rat cortical neurons. J Physiol 522, 3-17.
22. Kara T, Narkiewicz K & Somers VK (2003). Chemoreflexes - physiology and clinical implications. Acta Physiol Scand 177, 377-384.
23. 2-induced c-Fos expression in hypothalamic vasopressin containing neurons. Respir Physiol 129, 289-296.
24. Kinkead R, Genest SE, Gulemetova R, Lajeunesse Y, Laforest S, Drolet G & Bairam A (2005 a). Neonatal maternal separation and early life programming of the hypoxic ventilatory response in rats. Respir Physiol Neurobiol 149, 313-324.
25. Kinkead R, Gulemetova R & Bairam A (2005 b). Neonatal maternal separation enhances phrenic responses to hypoxia and carotid sinus nerve stimulation in the adult anesthetised rat. J Appl Physiol 99, 189-196.
26. 2 receptor and tyrosine hydroxylase mRNA expression levels in carotid body of rats. Can J Physiol Pharmacol 83, 76-84.
27. Larnicol N, Wallois F, Berquin P, Gros F & Rose D (1994). c-fos-like immunoreactivity in the cat's neuraxis following moderate hypoxia or hypercapnia. J Physiol (Paris) 88, 81-88.
28. Liu D, Caldji C, Sharma S, Plotsky PM & Meaney MJ (2000). Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol 12, 5-12.
29. A receptor subunits α1, α2, and α3 in the rat pre-Botzinger complex. J Appl Physiol 96, 1825-1831.
30. B receptor-activation inhibits GABAergic synaptic transmission in parvocellular neurones of rat hypothalamic paraventricular nucleus. J Neuroendocrinol 18, 177-186.
31. McCrimmon DR & Alheid GF (2004). Neonatal stress alters adult breathing. J Physiol 554, 591.
32. Mack SO, Kc P, Wu M, Coleman BR, Tolentino-Silva FP & Haxhiu MA (2002). Paraventricular oxytocin neurons are involved in neural modulation of breathing. J Appl Physiol 92, 826-834.
33. Mack SO, Wu M, Kc P & Haxhiu MA (2007). Stimulation of the hypothalamic paraventricular nucleus modulates cardiorespiratory responses via oxytocinergic innervation of neurons in pre-Botzinger complex. J Appl Physiol 102, 189-199.
34. B receptors in the rat central nervous system. J Comp Neurol 405, 299-321.
35. Mirescu C, Peters JD & Gould E (2004). Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7, 841-846.
36. Montandon G, Bairam A & Kinkead R (2006). Long-term consequences of neonatal caffeine on ventilation, occurrence of apneas, and hypercapnic chemoreflex in male and female rats. Pediatr Res 59, 519-524.
37. Narkiewicz K, van de Borne PJH, Pesek CA, Dyken ME, Montano N & Somers VK (1999). Selective potentiation of peripheral chemoreflex sensitivity in obstructive sleep apnea. Circulation 99, 1183-1189.
38. A receptor subunit mRNA levels in rat hippocampus. Brain Res Mol Brain Res 34, 29-37.
39. Paxinos G & Watson C (1998). The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
40. Plotsky PM & Meaney MJ (1993). Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18, 195-200.
41. Ponikowski P, Chua TP, Anker SD, Francis DP, Doehner W, Banasiak W, Poole-Wilson PA, Piepoli MF & Coats AJS (2001). Peripheral chemoreceptor hypersensitivity: An ominous sign in patients with chronic heart failure. Circulation 104, 544-549.
42. Powell FL, Milsom WK & Mitchell GS (1998). Time domains of the hypoxic ventilatory response. Respir Physiol 112, 123-134.
43. Reddy MK, Patel KP & Schultz HD (2005). Differential role of the paraventricular nucleus of the hypothalamus in modulating the sympathoexcitatory component of peripheral and central chemoreflexes. Am J Physiol Regul Integr Comp Physiol 289, R789-R797.
44. Rots NY, de Jong J, Workel JO, Levine S, Cools AR & De Kloet ER (1996). Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J Neuroendocrinol 8, 501-506.
45. Sawchenko PE, Li HY & Ericsson A (2000). Circuits and mechanisms governing hypothalamic responses to stress: A tale of two paradigms. Prog Brain Res 122, 61-78.
46. Schlenker EH (2005). Integration in the PVN: Another piece of the puzzle. Am J Physiol Regul Integr Comp Physiol 289, R653-R655.
47. Schlenker E, Barnes L, Hansen S & Martin D (2001). Cardiorespiratory and metabolic responses to injection of bicuculline into the hypothalamic paraventricular nucleus (PVN) of conscious rats. Brain Res 895, 33-40.
48. Schousboe A & Redburn DA (1995). Modulatory actions of gamma aminobutyric acid (GABA) on GABA type A receptor subunit expression and function. J Neurosci Res 41, 1-7.
49. Sieghart W (1995). Structure and pharmacology of g-aminobutyric acidA receptor subtypes. Pharmacol Rev 47, 181-234.
50. Smith ML & Pacchia CF (2007). Sleep apnoea and hypertension: Role of chemoreflexes in humans. Exp Physiol 92, 45-50.
51. Stocker SD, Keith KJ & Toney GM (2004). Acute inhibition of the hypothalamic paraventricular nucleus decreases renal sympathetic nerve activity and arterial blood pressure in water-deprived rats. Am J Physiol Regul Integr Comp Physiol 286, R719-R725.
52. 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.
53. Teppema LJ, Veening JG, Kranenburg A, Dahan A, Berkenbosch A & Olievier C (1997). Expression of c-fos in the rat brainstem after exposure to hypoxia and to normoxic and hyperoxic hypercapnia. J Comp Neurol 388, 169-190.
54. van Oers HJ, de Kloet ER & Levine S (1998 a). Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress. Brain Res Dev Brain Res 111, 245-252.
55. van Oers HJ, de Kloet ER, Li C & Levine S (1998 b). The ontogeny of glucocorticoid negative feedback: Influence of maternal deprivation. Endocrinology 139, 2838-2846.
56. B receptors modulate rapid neurotransmission from suprachiasmatic nucleus to parvocellular hypothalamic paraventricular nucleus neurons. Neuroscience 118, 49-58.
57. Yeh ER, Erokwu B, LaManna JC & Haxhiu MA (1997). The paraventricular nucleus of the hypothalamus influences respiratory timing and activity in the rat. Neurosci Lett 232, 63-66.
58. Younes M (2004). Role of arousals in the pathogenesis of obstructive sleep apnea. Am J Respir Crit Care Med 169, 623-633.
59. 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.