Role of paraventricular nucleus-projecting norepinephrine/epinephrine neurons in acute and chronic stress

European Journal of Neuroscience

Volumn 39, Issue 11, 2014, Pages 1903-1911

  Flak, Jonathan N ^a   Myers, Brent ^a   Solomon, Matia B ^a   Mcklveen, Jessica M ^a   Krause, Eric G ^a   Herman, James P ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Adrenocorticotrophic hormone; Corticotropin releasing hormone; Glucocorticoids; Nucleus of the solitary tract; Rats; Saporin

Indexed keywords

ADRENALIN; CORTICOSTERONE; CORTICOTROPIN; NORADRENALIN;

ACUTE STRESS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CHRONIC STRESS; CONTROLLED STUDY; HORMONE RELEASE; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMOBILIZATION STRESS; IMMUNOREACTIVITY; MALE; NERVE EXCITABILITY; NERVE FIBER; NERVE FUNCTION; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; RAT; WEIGHT GAIN; ADRENERGIC NERVE; ANIMAL; BLOOD; CYTOLOGY; DOPAMINERGIC NERVE CELL; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADRENERGIC FIBERS; ADRENOCORTICOTROPIC HORMONE; ANIMALS; CORTICOSTERONE; DOPAMINERGIC NEURONS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL;

EID: 84901691269     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12587     Document Type: Article

References (63)

1. Bienkowski, M.S. & Rinaman, L. (2008) Noradrenergic inputs to the paraventricular hypothalamus contribute to hypothalamic-pituitary-adrenal axis and central Fos activation in rats after acute systemic endotoxin exposure. Neuroscience, 156, 1093-1102.
2. Bornstein, S.R., Engeland, W.C., Ehrhart-Bornstein, M. & Herman, J.P. (2008) Dissociation of ACTH and glucocorticoids. Trends Endocrin. Met., 19, 175-180.
3. Buijs, R.M., la Fleur, S.E., Wortel, J., Van Heyningen, C., Zuiddam, L., Mettenleiter, T.C., Kalsbeek, A., Nagai, K. & Niijima, A. (2003) The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. J. Comp. Neurol., 464, 36-48.
4. Carvalho-Netto, E.F., Myers, B., Jones, K., Solomon, M.B. & Herman, J.P. (2011) Sex differences in synaptic plasticity in stress-responsive brain regions following chronic variable stress. Physiol. Behav., 104, 242-247.
5. Choi, D.C., Furay, A.R., Evanson, N.K., Ostrander, M.M., Ulrich-Lai, Y.M. & Herman, J.P. (2007) Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J. Neurosci., 27, 2025-2034.
6. Cole, R.L. & Sawchenko, P.E. (2002) Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J. Neurosci., 22, 959-969.
7. Cullinan, W.E. & Wolfe, T.J. (2000) Chronic stress regulates levels of mRNA transcripts encoding beta subunits of the GABA(A) receptor in the rat stress axis. Brain Res., 887, 118-124.
8. Cullinan, W.E., Herman, J.P., Battaglia, D.F., Akil, H. & Watson, S.J. (1995) Pattern and time-course of immediate-early gene-expression in rat-brain following acute stress. Neuroscience, 64, 477-505.
9. Cummings, S. & Seybold, V. (1988) Relationship of alpha-1- and alpha-2-adrenergic-binding sites to regions of the paraventricular nucleus of the hypothalamus containing corticotropin-releasing factor and vasopressin neurons. Neuroendocrinology, 47, 523-532.
10. Cunningham, E.T. Jr. & Sawchenko, P.E. (1988) Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J. Comp. Neurol., 274, 60-76.
11. Cunningham, E.T. Jr., Bohn, M.C. & Sawchenko, P.E. (1990) Organization of adrenergic inputs to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J. Comp. Neurol., 292, 651-667.
12. Daftary, S.S., Boudaba, C. & Tasker, J.G. (2000) Noradrenergic regulation of parvocellular neurons in the rat hypothalamic paraventricular nucleus. Neuroscience, 96, 743-751.
13. Dampney, R.A., Polson, J.W., Potts, P.D., Hirooka, Y. & Horiuchi, J. (2003) Functional organization of brain pathways subserving the baroreceptor reflex: studies in conscious animals using immediate early gene expression. Cell. Mol. Neurobiol., 23, 597-616.
14. Day, H.E., Campeau, S., Watson, S.J. Jr. & Akil, H. (1997) Distribution of alpha 1a-, alpha 1b- and alpha 1d-adrenergic receptor mRNA in the rat brain and spinal cord. J. Chem. Neuroanat., 13, 115-139.
15. Delfs, J.M., Zhu, Y., Druhan, J.P. & Aston-Jones, G.S. (1998) Origin of noradrenergic afferents to the shell subregion of the nucleus accumbens: anterograde and retrograde tract-tracing studies in the rat. Brain Res., 806, 127-140.
16. Fallon, J.H. & Loughlin, S.E. (1982) Monoamine innervation of the forebrain: collateralization. Brain Res. Bull., 9, 295-307.
17. Flak, J.N., Ostrander, M.M., Tasker, J.G. & Herman, J.P. (2009) Chronic stress-induced neurotransmitter plasticity in the PVN. J. Comp. Neurol., 517, 156-165.
18. Flak, J.N., Jankord, R., Solomon, M.B., Krause, E.G. & Herman, J.P. (2011) Opposing effects of chronic stress and weight restriction on cardiovascular, neuroendocrine and metabolic function. Physiol. Behav., 104, 228-234.
19. Grippo, A.J., Moffitt, J.A. & Johnson, A.K. (2002) Cardiovascular alterations and autonomic imbalance in an experimental model of depression. Am. J. Physiol.-Reg. I., 282, R1333-R1341.
20. Herman, J.P., Adams, D. & Prewitt, C. (1995) Regulatory changes in neuroendocrine stress-integrative circuitry produced by a variable stress paradigm. Neuroendocrinology, 61, 180-190.
21. Herman, J.P., Ostrander, M.M., Mueller, N.K. & Figueiredo, H. (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuro-psychoph., 29, 1201-1213.
22. Herman, J.P., Flak, J. & Jankord, R. (2008) Chronic stress plasticity in the hypothalamic paraventricular nucleus. Prog. Brain Res., 170, 353-364.
23. Imaki, T., Nahan, J.L., Rivier, C., Sawchenko, P.E. & Vale, W. (1991) Differential regulation of corticotropin-releasing factor mRNA in rat brain regions by glucocorticoids and stress. J. Neurosci., 11, 585-599.
24. Ippoliti, R., Lendaro, E., Bellelli, A. & Brunori, M. (1992) A ribosomal protein is specifically recognized by saporin, a plant toxin which inhibits protein synthesis. FEBS Lett., 298, 145-148.
25. Itoi, K., Suda, T., Tozawa, F., Dobashi, I., Ohmori, N., Sakai, Y., Abe, K. & Demura, H. (1994) Microinjection of norepinephrine into the paraventricular nucleus of the hypothalamus stimulates corticotropin-releasing factor gene expression in conscious rats. Endocrinology, 135, 2177-2182.
26. Jankord, R. & Herman, J.P. (2008) Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann. NY Acad. Sci., 1148, 64-73.
27. Jezova, D., Skultetyova, I., Tokarev, D.I., Bakos, P. & Vigas, M. (1995) Vasopressin and oxytocin in stress. Ann. NY Acad. Sci., 771, 192-203.
28. Khan, A.M., Ponzio, T.A., Sanchez-Watts, G., Stanley, B.G., Hatton, G.I. & Watts, A.G. (2007) Catecholaminergic control of mitogen-activated protein kinase signaling in paraventricular neuroendocrine neurons in vivo and in vitro: a proposed role during glycemic challenges. J. Neurosci., 27, 7344-7360.
29. Khan, A.M., Kaminski, K.L., Sanchez-Watts, G., Ponzio, T.A., Kuzmiski, J.B., Bains, J.S. & Watts, A.G. (2011) MAP kinases couple hindbrain-derived catecholamine signals to hypothalamic adrenocortical control mechanisms during glycemia-related challenges. J. Neurosci., 31, 18479-18491.
30. Kiss, A. & Aguilera, G. (1993) Regulation of the hypothalamic pituitary adrenal axis during chronic stress: responses to repeated intraperitoneal hypertonic saline injection. Brain Res., 630, 262-270.
31. Kitazawa, S., Shioda, S. & Nakai, Y. (1987) Catecholaminergic innervation of neurons containing corticotropin-releasing factor in the paraventricular nucleus of the rat hypothalamus. Acta Anat. (Basel), 129, 337-343.
32. Leibowitz, S.F., Diaz, S. & Tempel, D. (1989) Norepinephrine in the paraventricular nucleus stimulates corticosterone release. Brain Res., 496, 219-227.
33. Li, H.Y., Ericsson, A. & Sawchenko, P.E. (1996) Distinct mechanisms underlie activation of hypothalamic neurosecretory neurons and their medullary catecholaminergic afferents in categorically different stress paradigms. Proc. Natl. Acad. Sci. USA, 93, 2359-2364.
34. Liposits, Z., Sherman, D., Phelix, C. & Paull, W.K. (1986) A combined light and electron microscopic immunocytochemical method for the simultaneous localization of multiple tissue antigens. Tyrosine hydroxylase immunoreactive innervation of corticotropin releasing factor synthesizing neurons in the paraventricular nucleus of the rat. Histochemistry, 85, 95-106.
35. Loughlin, S.E., Foote, S.L. & Fallon, J.H. (1982) Locus coeruleus projections to cortex: topography, morphology and collateralization. Brain Res. Bull., 9, 287-294.
36. Ludwig, M. & Leng, G. (2006) Dendritic peptide release and peptide-dependent behaviours. Nat. Rev. Neurosci., 7, 126-136.
37. Madden, C.J., Ito, S., Rinaman, L., Wiley, R.G. & Sved, A.F. (1999) Lesions of the C1 catecholaminergic neurons of the ventrolateral medulla in rats using anti-DbetaH-saporin. Am. J. Physiol., 277, R1063-R1075.
38. Makino, S., Smith, M.A. & Gold, P.W. (1995) Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology, 136, 3299-3309.
39. Mamalaki, E., Kvetnansky, R., Brady, L.S., Gold, P.W. & Herkenham, M. (1992) Repeated immobilization stress alters tyrosine-hydroxylase, corticotropin-releasing hormone and corticosteroid receptor messenger-ribonucleic-acid levels in rat brain. J. Neuroendocrinol., 4, 689-699.
40. Maxwell, S. & Delaney, H. (1989) Designing Experiment and Analyzing Data: A Model Comparison Perspective. Wadsworth, Belmont, CA, USA.
41. McClave, J.T. & Dietrich, F. (1994) Statistics, 6th Edn. Macmillan College Publishing Company, Inc., Englewood Cliffs, NJ.
42. Mezey, E., Reisine, T.D., Brownstein, M.J., Palkovits, M. & Axelrod, J. (1984) Beta-adrenergic mechanism of insulin-induced adrenocorticotropin release from the anterior pituitary. Science, 4678, 1085-1087.
43. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, Sydney.
44. Rinaman, L. (2003) Hindbrain noradrenergic lesions attenuate anorexia and alter central cFos expression in rats after gastric viscerosensory stimulation. J. Neurosci., 23, 10084-10092.
45. Ritter, S., Bugarith, K. & Dinh, T.T. (2001) Immunotoxic destruction of distinct catecholamine subgroups produces selective impairment of glucoregulatory responses and neuronal activation. J. Comp. Neurol., 432, 197-216.
46. Ritter, S., Watts, A.G., Dinh, T.T., Sanchez-Watts, G. & Pedrow, C. (2003) Immunotoxin lesion of hypothalamically projecting norepinephrine and epinephrine neurons differentially affects circadian and stressor-stimulated corticosterone secretion. Endocrinology, 144, 1357-1367.
47. Sawchenko, P.E. (1988) Effects of catecholamine-depleting medullary knife cuts on corticotropin-releasing factor and vasopressin immunoreactivity in the hypothalamus of normal and steroid-manipulated rats. Neuroendocrinology, 48, 459-470.
48. Sawchenko, P.E. & Swanson, L.W. (1981) Central noradrenergic pathways for the integration of hypothalamic neuroendocrine and autonomic responses. Science, 214, 685-687.
49. Sawchenko, P.E. & Swanson, L.W. (1982) The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res., 257, 275-325.
50. Schiltz, J.C. & Sawchenko, P.E. (2007) Specificity and generality of the involvement of catecholaminergic afferents in hypothalamic responses to immune insults. J. Comp. Neurol., 502, 455-467.
51. Szafarczyk, A., Malaval, F., Laurent, A., Gibaud, R. & Assenmacher, I. (1987) Further evidence for a central stimulatory action of catecholamines on adrenocorticotropin release in the rat. Endocrinology, 121, 883-892.
52. Teppema, L.J., Veening, J.G., 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.
53. Ulrich-Lai, Y.M. & Engeland, W.C. (2002) Adrenal splanchnic innervation modulates adrenal cortical responses to dehydration stress in rats. Neuroendocrinology, 76, 79-92.
54. Ulrich-Lai, Y.M., Arnhold, M.M. & Engeland, W.C. (2006) Adrenal splanchnic innervation contributes to the diurnal rhythm of plasma corticosterone in rats by modulating adrenal sensitivity to ACTH. Am. J. Physiol.-Reg. I., 290, R1128-R1135.
55. Ulrich-Lai, Y.M., Christiansen, A.M., Ostrander, M.M., Jones, A.A., Jones, K.R., Choi, D.C., Krause, E.G., Evanson, N.K., Furay, A.R., Davis, J.F., Solomon, M.B., de Kloet, A.D., Tamashiro, K.L., Sakai, R.R., Seeley, R.J., Woods, S.C. & Herman, J.P. (2011a) Pleasurable behaviors reduce stress via brain reward pathways. Proc. Natl. Acad. Sci. USA, 107, 20529-20534.
56. Ulrich-Lai, Y.M., Jones, K.R., Ziegler, D.R., Cullinan, W.E. & Herman, J.P. (2011b) Forebrain origins of glutamatergic innervation to the rat paraventricular nucleus of the hypothalamus: differential inputs to the anterior versus posterior subregions. J. Comp. Neurol., 519, 1301-1319.
57. Verkuyl, J.M., Hemby, S.E. & Joels, M. (2004) Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur. J. Neurosci., 20, 1665-1673.
58. Watanabe, Y., McKittrick, C.R., Blanchard, D.C., Blanchard, R.J., McEwen, B.S. & Sakai, R.R. (1995) Effects of chronic social stress on tyrosine hydroxylase mRNA and protein levels. Brain Res. Mol. Brain Res., 32, 176-180.
59. Wotjak, C.T., Ganster, J., Kohl, G., Holsboer, F., Landgraf, R. & Engelmann, M. (1998) Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons. Neuroscience, 85, 1209-1222.
60. Wrenn, C.C., Picklo, M.J., Lappi, D.A., Robertson, D. & Wiley, R.G. (1996) Central noradrenergic lesioning using anti-DBH-saporin: anatomical findings. Brain Res., 740, 175-184.
61. Zhang, R., Jankord, R., Flak, J.N., Solomon, M.B., D'Alessio, D.A. & Herman, J.P. (2010) Role of glucocorticoids in tuning hindbrain stress integration. J. Neurosci., 30, 14907-14914.
62. Ziegler, D.R., Cass, W.A. & Herman, J.P. (1999) Excitatory influence of the locus coeruleus in hypothalamic-pituitary-adrenocortical axis responses to stress. J. Neuroendocrinol., 11, 361-369.
63. Ziegler, D.R., Cullinan, W.E. & Herman, J.P. (2005) Organization and regulation of paraventricular nucleus glutamate signaling systems: N-methyl-D-aspartate receptors. J. Comp. Neurol., 484, 43-56.