Cited by 73Stress Responses and CortisolNeuropeptides and Animal PhysiologyNeuroendocrine regulation and behavior

The Effect of Stressor Controllability on Stress‐Induced Neuropeptide mRNA Expression within the Paraventricular Nucleus of the Hypothalamus

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Helmreich, Watkins, Deak, Maier, Akil, Watson·1999·Journal of Neuroendocrinology

Abstract

Many stressors elicit changes in corticotrophin (CRH), enkephalin (ENK), and neurotensin (NT) mRNA levels within the medial parvocellular region of the paraventricular nucleus of the hypothalamus (mpPVN), and the pattern of changes in mRNA levels appears to depend on the physical characteristics of the stressor. We questioned whether psychologically distinct stressors would cause different patterns of neuropeptide mRNA expression within the PVN. Psychologically distinct stressors were created by employing a paradigm of escapable (controllable) vs non‐escapable (yoked) tail shock. An adult male rats could terminate the stress stimulus by performing wheel‐turning behaviour; his behaviour also terminated the stress for his yoked partner, who had no control over the termination of the shock. Four h post‐stress, brains were collected and processed for in‐situ hybridization histochemistry. Tail‐shock stress stimulated a significant increase in CRH, ENK, and NT mRNA levels within the mpPVN. The number of CRH identified neurones coexpressing AVP mRNA was also significantly elevated in both stress groups. Moreover, the pattern and magnitude of the stress‐induced increases in mRNA was similar in both stress groups. Additionally, no stress‐induced changes in CRH mRNA levels were observed in the central nucleus of the amygdala. In sum, two psychologically distinct stressors, escapable vs yoked tail shock stress, stimulated similar increases in CRH, NT, ENK, and AVP mRNA levels within the mpPVN. These results suggest that physical attributes of a stress, rather than psychological, may be the more important factors in determining the PVN mRNA response.

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Research works printed but not linked: 27

  1. Young E, Haskett R, Grunhaus L, Pande A, Weinberg V, Watson S, Akil H. Increased activation of the hypothalamic-pituitary-adrenal axis 1 Herman J, Prewitt M-F, Cullinan W. Neuronal circuit regulation of the in depressed patients. Arch Gen Psychiatry 1994; 51: 701-707.
  2. Matthews J, Akil H, Greden J, Charney D, Weinberg V, Rodenbaum A, 1996; 10: 371-394.
  3. Watson S. b-Endorphin/b-Lipotropin immunoreactivity in endogenous 2 Li H-Y, Ericsson A, Sawchenko P. Distinct mechanisms underlie activa- depression. Arch Gen Psychiatry 1986; 43: 374-381. tion of hypothalamic neurosecretory neurons and their medullary catech- 27
  4. Purba J, Hoogendijk W, Hofman M, Swaab D. Increased number of olaminergic afferents in categorically different stress paradigms. Proc vasopressin-and oxytocin-expressing neurons in the paraventricular Natl Acad Sci 1996; 93: 2359-2364. nucleus of the hypothalamus in depression. Arch Gen Psychiatry 1996;
  5. Modell S, Yassouridis A, Huber J, Holsboer F. Corticosteroid receptor Endocrine Rev 1986; 7: 351-378. function is decreased in depressed patients. Neuroendo 1997; 65: 216-222.
  6. Ceccatelli S, Eriksson M, Ho ¨kfelt T. Distribution and coexistence of 30 Romero M, Plotsky P, Sapolsky R. Patterns of adrenocorticotropin corticotropin-releasing factor-, neurotensin-, enkephalin-, cholecysto- secretagogue release with hypoglycemia, novelty, and restraint after kinin-, galanin-, and vasoactive intestinal polypeptide/peptide histidine colchicine blockade of axonal transport. Endocrinol 1993; 132:. 199. isoleucine-like peptides in the parvocellular part of the paraventricular 31 Romero L, Levine S, Sapolsky R. Patterns of adrenocorticotropin nucleus. Neuroendocr 1989; 49: 309-323. secretagog release in response to social interactions and various degrees 6 Merchenthaler I. Enkephalin-immunoreactive neurons in the parvicellular of novelty. Psychoneuroendo 1995; 20: 183-191. suddivisions of the paraventricular nucleus project to the external zone 32 Darlington D, Baraclough C, Gann D. Hypotensive hemorrhage elevates of the median eminence. J Comp Neurol 1992; 326: 112-120. corticotropin-releasing hormone messenger ribonucleic acid (mRNA) but 7 Pretel S, Piekut D. Coexistence of corticotropin-releasing factor and not vasopressin mRNA in the rat hypothalamus. Endocrinol 1992; 130: enkephalin in the paraventricular nucleus of the rat. J Comp Neurol 1281-1288. 1990; 294: 192-201.
  7. Miller A, Spencer R, Pulera M, Kang S, McEwen B, Stein M. Adrenal 8 Plotsky P, Bruhn T, Vale W. Evidence for multifactoral regulation of steroid receptor activation in rat brain and pituitary following dexametha- the adrenocorticotropin secretory response to hemodynamic stimuli. sone: Implications for the dexamethaone suppression test. Biol Psychiatry Endocrinol 1985; 116: 633-639. 1992; 32: 850-869.
  8. Plotsky P, Bruhn T, Vale W. Hypophysiotropic regulation of adrenocort- 34 Maier S. Learned helplessness and animal models of depression. Prog icotropin secretion in response to insulin-induced hypoglycemia. Neuro-Psycholopharmacol Biol Psychiat 1984; 8: 435-446. Endocrinol 1985; 117: 323-329.
  9. Schmidt E, Binnekade R, Janszen A, Tilders F. Short stressor induced 10 Watts A. Ether anesthesia diffentially affects the content of prepro- long-lasting increases of vasopressin stores in hypothalamic corticotropin- corticotropin-releasing hormone, prepro-neurotensin/neuromedin N and releasing hormone (CRH ) neurons in adult rats. J Neuroendocrinol 1996; prepro-enkephalin mRNAs in the hypothalamic paraventricular nucleus 8: 703-712. of the rat. Brain Res 1991; 544: 353-357.
  10. Ma X-M, Levy A, Lightman S. Emergence of an isolated arginine 11 Ceccatelli S, Orazzo C. Effect of different types of stressors on peptide vasopressin (AVP) response to stress after repeated restraint: a study of messenger ribonucleic acids in the hypothalamic paraventricular nucleus. both AVP and corticotropin-releasing hormone messenger ribonucleic Acta Endocrinol 1993; 128: 485-492. acid (RNA) and heteronucleur RNA. Endocrinol 1997; 138: 4351-4357.
  11. Maier S, Drugan R, Grau J. Controllability, coping behavior, and stress- regulating adrenocorticotropic hormone secretion? J Neurosci 1996; 16: induced analgesia in the rat. Pain 1982; 12: 47-56. 7725-7732.
  12. Telner J, Merali Z, Singhal R. Stress controllability and plasma prolactin 38 Imaki T, Naruse M, Harada S, Chikada N, Imaki J, Onodera H, levels in the rat. Psychoneuroendo 1982; 7: 361-364.
  13. Murison R, Isaksen E. Gastric ulceration and adrenocortical activity Demura H, Vale W. Corticotropin-releasing factor up-regulates its own receptor mRNA in the paraventricular nucleus of the hypothalamus. 52 Watts A, Sanchez-Watts G. Physiological regulation of peptide messenger Mol Brain Res 1996; 38: 166-170. RNA colocalization in rat hypothalamic paraventricular medial parvicel- 39
  14. Nicot A, Rowe W, de Kloet E, Betancur C, Jessop D, Lightman S, lular neurons. J Comp Neurol 1995; 352: 501-514.
  15. Quirion R, Rostene W, Berod A. Endogenous neurotensin regulates 53 Watkins L, Wiertelak E, Maier S. The amygdala is necessary for the hypothalamic-pituitary-adrenal axis activity and peptidergic neurons in expresssion of conditioned but not unconditioned analgesia. Behav the rat hypothalamic paraventricular nucleus. J Neuroendo 1997; 9: Neuroscience 1993; 107: 402-405. 263-269.
  16. Koob G, Heinrichs S, Pich E, Menzaghi F, Baldwin H, Miczek K, 40 Rowe W, Viau V, Meaney M, Quirion R. Stimulation of CRH-mediated Britton K. The role of corticotropin-releasing factor in behavioral ACTH secretion by central administration of neurotensin: evidence for responses to stress. In: Chadwick DJ, Marsh J, Ackrill K, eds. the participation of the paraventricular nucleus. J Neuroendo 1995; Corticotropin-releasing Factor (Ciba Foundation Symposium 172). 7: 109-117. Chichester: Wiley, 1993: 277-295.
  17. Rowe W, Nicot A, Sharma S, Gully D, Walker C, Rostene W, Meaney 55 Maier S, Grahn R, Kalman B, Sutton L, Wiertelak E, Watkins L. The M, Quirion R. Central administration of the neurotensin receptor role of the amygdala and dorsal raphe nucleus in mediating the behavioral antagonist, SR48692, modulates diurnal and stress-related hypothalamic- consequences of inescapable shock. Behav Neuroscience 1993; 107: pituitary-adrenal acitivity. Neuroendocrinology 1997; 66: 75-85. 377-388.
  18. Nicholson S, Adrian T, Gillham B, Jones M, Bloom S. Effect of 56 Mamalaki E, Kvetnansky R, Brady LS, Gold PW, Herkenham M. hypothalamic neuropeptides on corticotrophin release form quarters of Repeated immobilization stress alters tyrosine hydroxylase, corticotropin- rat anterior pituitary gland in vitro. J Endocr 1984; 100: 219-226. releasing hormone and corticosteroid receptor messenger ribonucleic acid 43 Brooks N, Challis J. Effects of CRF, AVP, and opioid peptides on levels in rat brain. J Neuroendocrinol 1992; 4: 689-699. pituitary-adrenal responses in sheep. Peptides 1989; 10: 1291-1293.
  19. Makino S, Gold P, Schulkin J. Effects of corticosterone on CRH mRNA 44 Giusti M, Marini G, Uggias B, Sessarego P, Besser G, Grossman A, and content in the bed nucleus of the stria terminalis: comparison with Giordano G. The effect of a met-enkephalin analogue on growth hor- the effects on the central nucleus of the amygdala and the paraventricular mone, prolactin, gonadotropins, cortisol, and thyroid stimulating hor- nucleus of the hypothalamus. Brain Res 1994; 657: 141-149. mone in healthy elderly men. Acta Endocrinologica 1992; 127: 205-209.
  20. Iyengar S, Kim H, Wood P. Kappa opiate agonists modulate the induces differential patterns of c-fos activation in rat brain: implications hypothalamic-pituitary-adrenocortical axis in the rat. J Pharm Exp for mechanism of action. In: Society for Neuroscience Annual Meeting, Therapeutics 1986; 238: 429-436.
  21. Allolio B, Deuss U, Kaulen D, Leonhardt U, Kallabis D, Hamel E, 59 Grahn R, Kalman B, Brennan F, Watkins L, Maier S. The elevated Winkelmann W. FK 33-824, a Met-Enkaphalin analog, blocks cortico- plus-maze is not sensitive to the effect of stressor controllability in rats. tropin-releasing hormone-induced adrenocorticotropin secretion in Pharm Biochem Behav 1995; 52: 565-570. normal subjects but not in patients with Cushing's disease. Endocrinology 60
  22. Schafer K-H, Herman J, Watson S. In situ hybridization histochemistry. 1986; 63: 1427-1431. In: London E, ed. Imaging Drug Action in the Brain. Boca Raton: CRC 47
  23. Buckingham J, Cooper T. Differences in hypothalamo-pituitary- Press, 1993: 337-377. adrenocortical activity in the rat after acute and prolonged treatment 61 Alexander M, Miller M, Dorsa D, Bullock B, Melloni R, Dobner P, with morphine. Neuroendocrinology 1984; 38: 411-417.
  24. Leeman S. Distribution of neurotensin/neuromedi N mRNA in rat 48 Sawchenko P. Adrenalectomy-induced enhancement of CRF and vaso- forebrain: Unexpected abundance in hippocampus and subiculum. Proc pressin immunoreactivity in parvocellular neurosecretory neurons: ana- Natl Acad Sci 1989; 86: 5202-5206.
  25. tomic, peptide, and steroid specificity. J Neurosci 1987; 7: 1093-1106.
  26. Curran E, Watson S. Dopamine receptor mRNA expression patterns by 49 Swanson L, Simmons D. Differential steroid hormone and neural influ- opioid peptide cells in the nucleus accumbens of the rat: A double in situ ences on peptide mRNA levels in CRH cells of the paraventricular hybiridization study. J Comp Neurol 1995; 361: 57-76. nucleus: a hybridization histochemical study in the rat. J Comp Neurol 63 Day HEW, Akil H. Differential pattern of c-fos mRNA in rat brain 1989; 285: 413-435. following central and systemic adminstration of interleukin-1-Beta: 50
  27. Watts A, Sanchez-Watts G. Region-specific regulation of neuropeptide implications for mechanism of action. Neuroendocrinol 1996; 63: 207-218. mRNAs in rat limbic forebrain neurones by aldosterone and corticos- 64 Herman J, Cullinan W, Watson S. Involvement of the bed nucleus of terone. J Physiol 1995; 3: 721-736. the stria terminalis in tonic regulation of paraventricular hypothalamic 51 Swanson L. Biochemical switching in hypothalamic circuits mediating responses to stress. Prog Brain Res 1991; 87: 181-200. CRH and AVP mRNA expression. J Neuroendocrinol 1994; 6: 433-442.

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Authors
Helmreich, Watkins, Deak, Maier, Akil, & Watson
Affiliations
  • University of Michigan (US)
  • University of Colorado Boulder (US)
Venue
Journal of Neuroendocrinology
Publisher
Wiley
Published
1999-02
Volume
11
Issue
2
Pages
121-128
ISSN
  • 0953-8194 (ISSN-L)
  • 1365-2826
OpenAlex
W1501439639
Cited by
73
References
2
Citations by year
2026: 1 · 2025: 1 · 2023: 2 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 2 · 2016: 1 · 2015: 1 · 2014: 3 · 2013: 1 · 2012: 2
FWCI
1.25
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroendocrinology (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • Deep Blue (University of Michigan) (submittedVersion, public-domain)
Funders
  • Department of Science and Technology, Ministry of Science and Technology, India
  • National Institutes of Health (5f32mh010715-03)
  • National Institute of Mental Health (MH 42251, MH 50479, P01MH042251, MH10715)
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords
stressor controllability, paraventricular nucleus, corticotropin-releasing factor, enkephalin, neurotensin, vasopressin, central amygdala, stress response
MeSH terms
Animals, Arginine Vasopressin, Corticosterone, Corticotropin-Releasing Hormone, Enkephalins, Male, Neuropeptides, Neurotensin, Paraventricular Hypothalamic Nucleus, RNA, Messenger, Stress, Physiological, Gene Expression, Rats, Sprague-Dawley, In Situ Hybridization, Rats

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