The effect of air puff stress on c-Fos expression in rat hypothalamus and brainstem: Central circuitry mediating sympathoexcitation and baroreflex resetting

European Journal of Neuroscience

Volumn 39, Issue 9, 2014, Pages 1429-1438

  Furlong, Teri M ^a   Mcdowall, Lachlan M ^a   Horiuchi, Jouji ^a   Polson, Jaimie W ^a   Dampney, Roger A L ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Paraventricular nucleus; Periaqueductal gray; Perifornical area; Rostral ventromedial medulla; Sympathetic activity

Indexed keywords

CATECHOLAMINE; PROTEIN C FOS;

AIR PUFF STRESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN STEM; BRAIN TISSUE; CATECHOLAMINE SYNTHESIS; CELL ACTIVATION; CONTROLLED STUDY; DORSOMEDIAL HYPOTHALAMUS; HYPOTENSION; HYPOTHALAMUS; MENTAL STRESS; NERVE PROJECTION; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PERIAQUEDUCTAL GRAY MATTER; PERIFORNICAL AREA; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ROSTRAL VENTROLATERAL MEDULLA; SOLITARY TRACT NUCLEUS; SYMPATHETIC NERVE CELL; SYMPATHETIC REFLEX; SYMPATHETIC TONE; ADRENERGIC SYSTEM; ANIMAL; BLOOD PRESSURE; METABOLISM; NERVE CELL; SPRAGUE DAWLEY RAT;

ANIMALS; BAROREFLEX; BLOOD PRESSURE; BRAIN STEM; HYPOTHALAMUS; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; SYMPATHETIC NERVOUS SYSTEM;

EID: 84899978613     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12521     Document Type: Article

References (55)

1. Bourassa, E.A., Sved, A.F. & Speth, R.C. (2009) Angiotensin modulation of rostral ventrolateral medulla (RVLM) in cardiovascular regulation. Mol. Cell. Endocrinol., 302, 167-175.
2. Buller, K.M., Dayas, C.V. & Day, T.A. (2003) Descending pathways from the paraventricular nucleus contribute to the recruitment of brainstem nuclei following a systemic immune challenge. Neuroscience, 118, 189-203.
3. Carrive, P. (1993) The periaqueductal gray and defensive behavior: functional representation and neuronal organization. Behav. Brain Res., 58, 27-47.
4. Carrive, P. & Gorissen, M. (2008) Premotor sympathetic neurons of conditioned fear in the rat. Eur. J. Neurosci., 28, 428-446.
5. Casto, R., Nguyen, T. & Printz, M.P. (1989) Characterization of cardiovascular and behavioral responses to alerting stimuli in rats. Am. J. Physiol. Reg. I., 256, R1121-R1126.
6. Chan, R.K. & Sawchenko, P.E. (1994) Spatially and temporally differentiated pattern of c-fos expression in brainstem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J. Comp. Neurol., 348, 433-460.
7. Chan, R.K., Jarvina, E.V. & Sawchenko, P.E. (2000) Effects of selective sinoaortic denervations on phenylephrine-induced activational responses in the nucleus of the solitary tract. Neuroscience, 101, 165-178.
8. Ciriello, J., Hochstenbach, S.L. & Roder, S. (1993). Central projections of baroreceptor and chemoreceptor afferent fibers in the rat. In Barraco, I.R.A. (Ed), Nucleus of the Solitary Tract. CRC Press, Boca Raton, pp. 35-50.
9. Cox, B.F. & Brody, M.J. (1989) Subregions of rostral ventral medulla control arterial pressure and regional hemodynamics. Am. J. Physiol. Reg. I., 257, R635-R640.
10. Cox, B.F. & Brody, M.J. (1991) Tonic control of arterial pressure and regional hemodynamics by supra-medullary sites. Clin. Exp. Hypertens. A., 13, 197-218.
11. Dampney, R.A.L. (1994) Functional organization of central pathways regulating the cardiovascular system. Physiol. Rev., 74, 323-364.
12. Dampney, R.A.L., Horiuchi, J. & McDowall, L.M. (2008) Hypothalamic mechanisms coordinating cardiorespiratory function during exercise and defensive behaviour. Auton. Neurosci. Basic, 142, 3-10.
13. Daubert, D.L., McCowan, M., Erdos, B. & Scheuer, D.A. (2012) Nucleus of the solitary tract catecholaminergic neurons modulate the cardiovascular response to psychological stress in rats. J. Physiol., 590, 4881-4895.
14. Dayas, C.V. & Day, T.A. (2001) Opposing roles for medial and central amygdala in the initiation of noradrenergic cell responses to a psychological stressor. Eur. J. Neurosci., 15, 1712-1718.
15. Dayas, C.V., Buller, K.M., Crane, J.W., Xu, Y. & Day, T.A. (2001a) Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. Eur. J. Neurosci., 14, 1143-1152.
16. Dayas, C.V., Buller, K.M. & Day, T.A. (2001b) Medullary neurones regulate hypothalamic corticotropin-releasing factor cell responses to an emotional stressor. Neuroscience, 105, 707-719.
17. Dayas, C.V., Buller, K.M. & Day, T.A. (2004) Hypothalamic paraventricular nucleus neurons regulate medullary catecholamine cell responses to restraint stress. J. Comp. Neurol., 478, 22-34.
18. DiMicco, J.A., Samuels, B.C., Zaretskaia, M.V. & Zaretsky, D.V. (2002) The dorsomedial hypothalamus and the response to stress: part renaissance, part revolution. Pharmacol. Biochem. Be., 71, 469-480.
19. Donoghue, S., Fox, R.E., Kidd, C. & McWilliam, P.N. (1981) The terminations and secondary projections of myelinated and non-myelinated fibres of the aortic nerve in the cat. Q. J. Exp. Physiol., 66, 405-422.
20. Donoghue, S., Felder, R.B., Jordan, D. & Spyer, K.M. (1984) The central projections of carotid baroreceptors and chemoreceptors in the cat: a neurophysiological study. J. Physiol., 347, 397-409.
21. Farkas, E., Jansen, A.S. & Loewy, A.D. (1997) Periaqueductal gray matter projection to vagal preganglionic neurons and the nucleus tractus solitarius. Brain Res., 764, 257-261.
22. Ferguson, I.A., Hardman, C.D., Marotte, L.R., Salardini, A., Halasz, P., Vu, D. & Waite, P.M.E. (1999) Serotonergic neurons in the brainstem of the wallaby, macropus eugenii. Brain Res., 411, 535-549.
23. Furlong, T.M. & Carrive, P. (2007) Neurotoxic lesions centered on the perifornical hypothalamus abolish the cardiovascular and behavioral responses of conditioned fear to context but not of restraint. Brain Res., 1128, 107-119.
24. Furlong, T.M., Vianna, D.M., Liu, L. & Carrive, P. (2009) Hypocretin/orexin contributes to the expression of some but not all forms of stress and arousal. Eur. J. Neurosci., 30, 1603-1614.
25. Furlong, T.M., Cole, S., Hamlin, A.S. & McNally, G.P. (2010) The role of prefrontal cortex in predictive fear learning. Behav. Neurosci., 124, 574-586.
26. Gibbs, D.M. (1986) Oxytocin inhibits ACTH and peripheral catecholamine sretion in the urethane-anesthetized rat. Regul. Peptides, 14, 125-132.
27. Goodchild, A.K. & Moon, E.A. (2009) Maps of cardiovascular and respiratory regions of rat ventral medulla: focus on the caudal medulla. J. Chem. Neuroanat., 38, 209-221.
28. Gordon, F.J. & McCann, L.A. (1988) Pressor responses evoked by microinjections of L-glutamate into the caudal ventrolateral medulla of the rat. Brain Res., 457, 251-258.
29. Guyenet, P.G. (2006) The sympathetic control of blood pressure. Nat. Rev. Neurosci., 7, 335-346.
30. Halasz, P. & Martin, P. (1985). Magellan, A Program for the Quantitative Analysis of Histological Sections. University of New South Wales, Sydney.
31. Iigaya, K., Muller-Ribeiro, F.C., Horiuchi, J., McDowall, L.M., Nalivaiko, E., Fontes, M.A.P. & Dampney, R.A.L. (2012) Blockade of orexin receptors with Almorexant reduces cardiorespiratory responses evoked from the hypothalamus but not baro- or chemoreceptor reflex responses. Am. J. Physiol. Reg. I., 303, R1011-R1022.
32. Jansen, A.S., Wessendorf, M.W. & Loewy, A.D. (1995) Transneuronal labeling of CNS neuropeptide and monoamine neurons after pseudorabies virus injections into the stellate ganglion. Brain Res., 683, 1-24.
33. Kanbar, R., Orea, V., Barres, C. & Julien, C. (2007) Baroreflex control of renal sympathetic nerve activity during air-jet stress in rats. Am. J. Physiol. Reg. I., 292, R362-R367.
34. LeDoux, J.E., Iwata, J., Cicchetti, P. & Reis, D.J. (1988) Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J. Neurosci., 8, 2517-2529.
35. Li, Y.W. & Dampney, R.A.L. (1994) Expression of Fos-like protein in brain following sustained hypertension and hypotension in conscious rabbits. Neuroscience, 61, 613-634.
36. Lovick, T.A. (1993) The periaqueductal gray-rostral medulla connection in the defence reaction: efferent pathways and descending control mechanisms. Behav. Brain Res., 58, 19-25.
37. McDougall, S.J., Widdop, R.E. & Lawrence, A.J. (2004) Medial prefrontal cortical integration of psychological stress in rats. Eur. J. Neurosci., 20, 2430-2440.
38. McDowall, L.M., Horiuchi, J., Killinger, S. & Dampney, R.A.L. (2006) Modulation of the baroreceptor reflex by the dorsomedial hypothalamic nucleus and perifornical area. Am. J. Physiol. Reg. I., 290, R1020-R1026.
39. Mifflin, S.W., Spyer, K.M. & Withington-Wray, D.J. (1988) Baroreceptor inputs to the nucleus tractus solitarius in the cat: modulation by the hypothalamus. J. Physiol., 399, 369-387.
40. Palmer, A.A. & Printz, M.P. (1999) Strain differences in Fos expression following airpuff startle in spontaneously hypertensive and Wistar Kyoto rats. Neuroscience, 89, 965-978.
41. Paxinos, G. & Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates. Elsevier, Amsterdam.
42. Sawchenko, P.E., Brown, E.R., Chan, R.K., Ericsson, A., Li, H.Y., Roland, B.L. & Kovacs, K.J. (1996) The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. Prog. Brain Res., 107, 201-222.
43. Sawchenko, P.E., Li, H.Y. & Ericsson, A. (2000) Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms. Prog. Brain Res., 122, 61-78.
44. Schramm, L.P., Strack, A.M., Platt, K.B. & Loewy, A.D. (1993) Peripheral and central pathways regulating the kidney: a study using pseudorabies virus. Brain Res., 616, 251-262.
45. Schreihofer, A.M. & Guyenet, P.G. (2000) Sympathetic reflexes after depletion of bulbospinal catecholaminergic neurons with anti-DbetaH-saporin. Am. J. Physiol. Reg. I., 279, R729-R742.
46. Spencer, S.J. & Day, T.A. (2004) Role of catecholaminergic inputs to the medial prefrontal cortex in local and subcortical expression of Fos after psychological stress. J. Neurosci. Res., 78, 279-288.
47. Spencer, S.J., Fox, J.C. & Day, T.A. (2004) Thalamic paraventricular nucleus lesions facilitate central amygdala neuronal responses to acute psychological stress. Brain Res., 997, 234-237.
48. Spencer, S.J., Buller, K.M. & Day, T.A. (2005) Medial prefrontal cortex control of the paraventricular hypothalamic nucleus response to psychological stress: possible role of the bed nucleus of the stria terminalis. J. Comp. Neurol., 481, 363-376.
49. Strack, A.M., Sawyer, W.B., Hughes, J.H., Platt, K.B. & Loewy, A.D. (1989) A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections. Brain Res., 491, 156-162.
50. Talman, W.T. & Lin, L.-H. (2013) Sudden death following selective neuronal lesions in the rat nucleus tractus solitarii. Auton. Neurosci. Basic, 175, 9-16.
51. Thrivikraman, K.V., Nemeroff, C.B. & Plotsky, P.M. (2000) Sensitivity to glucocorticoid-mediated fast-feedback regulation of the hypothalamic- pituitary-adrenal axis is dependent upon stressor specific neurocircuitry. Brain Res., 870, 87-101.
52. Ulrich-Lai, Y.M. & Herman, J.P. (2009) Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci., 10, 397-409.
53. Vianna, D.M. & Carrive, P. (2010) Cardiovascular and behavioural responses to conditioned fear and restraint are not affected by retrograde lesions of A5 and C1 bulbospinal neurons. Neuroscience, 166, 1210-1218.
54. Walker, P. & Carrive, P. (2003) Role of ventrolateral periaqueductal gray neurons in the behavioral and cardiovascular responses to contextual conditioned fear and poststress recovery. Neuroscience, 116, 897-912.
55. Weston, M., Wang, H., Stornetta, R.L., Sevigny, C.P. & Guyenet, P.G. (2003) Fos expression by glutamatergic neurons of the solitary tract nucleus after phenylephrine-induced hypertension in rats. J. Comp. Neurol., 460, 525-541.