Skip to main content
SpringerLink
Log in

Neural circuitry in the regulation of adrenal corticosterone rhythmicity

  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Adrenal cortical secretion of glucocorticoids is an essential adaptive response of an organism to stress. Although the hypothalamic-pituitary-adrenal axis regulates the adrenal cortex via release of ACTH, there is strong evidence supporting a role for sympathetic innervation in modulating adrenal glucocorticoid secretion. The dissociation between changes in ACTH and glucocorticoids under non-stress and stress conditions has reinforced the concept that neural control of the adrenal cortex acts to modulate steroidogenic responses to circulating ACTH. A dual control of the adrenal cortex has been implicated in the prominent circadian rhythm in glucocorticoids. However, the central neural substrate for circadian changes in glucocorticoids that are mediated by peripheral neural innervation of the adrenal cortex has not been conclusively delineated. The hypothesis to be addressed is that neurons in the paraventricular nucleus of the hypothalamus receive input from the suprachiasmatic nucleus and project to sympathetic preganglionic neurons in the spinal cord to provide inhibitory and excitatory input to the adrenal cortex that drives the circadian rhythm. This review examines anatomical and physiological evidence that forms the basis for this putative neural circuit.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Dallman, M. F., Engeland, W. C., Rose, J. C., Wilkinson, C. W., Shinsako, J., and Siedenburg, F. (1978). Am. J. Physiol. 235, R210–218.

    PubMed  CAS  Google Scholar 

  2. Szafarczyk, A., Alonso, G., Ixart, G., Malaval, F., Nouguier-Soule, J., and Assenmacher, I. (1980). Am.J.Physiol. 239, E482-E489.

    PubMed  CAS  Google Scholar 

  3. Kalsbeek, A., Heerikhuize, J. J. v., Wortel, J., and Buijs, R. M. (1996). J. Neuroscience 16, 5555–5565.

    CAS  Google Scholar 

  4. Morimoto, Y., Arisue, K., and Yamamura, Y. (1977). Neuroendocrinology 23, 212–222.

    PubMed  CAS  Google Scholar 

  5. Moore, R. Y. and Eichler, V. B. (1972). Brain Res. 42, 201–206.

    PubMed  CAS  Google Scholar 

  6. Krieger, D. T., Hauser, H., and Krey, L. C. (1977). Science 197, 398–399.

    PubMed  CAS  Google Scholar 

  7. Dallman, M. F., Darlington, D. N., Suemara, S., Cascio, C. S., and Levin, N. (1989). Acta Physiol. Scand. 136(Suppl. 583), 27–34.

    Google Scholar 

  8. De Kloet, E. R. (1991). Front. Neuroendocrinol. 12, 95–164.

    Google Scholar 

  9. Kaneko, M., Hiroshige, T., Shinsako, J., and Dallman, M. F. (1980). Am. J. Physiol. 239, R309-R316.

    PubMed  CAS  Google Scholar 

  10. Watts, A. G., Tanimura, S., and Sanchez-Watts, G. (2004). Endocrinology 145, 529–540.

    PubMed  CAS  Google Scholar 

  11. Kwak, S. P., Young, E. A., Morano, I., Watson, S. J., and Akil, H. (1992). Neuroendocrinology 55, 74–83.

    PubMed  CAS  Google Scholar 

  12. Honma, K.-I., Noe, Y., Honma, S., Katsuno, Y., and Hiroshige, T. (1992). Am. J. Physiol. (Endo. Metab. Physiol.) 262, E948–955.

    CAS  Google Scholar 

  13. Ixart, G., Conte-Devoix, B., Szafarczyk, A., Malaval, F., Oliver, C., and Assenmacher, I. (1985). C.R. Acad. Sc. Paris 301, 659–664.

    CAS  Google Scholar 

  14. Carnes, M., Lent, S. J., Erisman, S., Barksdale, C. M., and Feyzi, J. (1989). Life Sci. 45, 1049–1056.

    PubMed  CAS  Google Scholar 

  15. Bagdy, G., Chrousos, G. P., and Calogero, A.E. (1991). Neuroendocrinology 53, 573–578.

    PubMed  CAS  Google Scholar 

  16. Kaneko, M., Kaneko, K., Shinsako, J., and Dallman, M. F. (1981). Endocrinology 109, 70–75.

    PubMed  CAS  Google Scholar 

  17. Holgert, H., Aman, K., Cozzari, C., et al. (1995). Neuroreport 6, 2576–2580.

    PubMed  CAS  Google Scholar 

  18. Kondo, H. (1985). Arch. Histo. Jpn. 48, 453–481.

    CAS  Google Scholar 

  19. Holgert, H., Dagerlind, A., and Hokfelt, T. (1998). Horm. Metab. Res. 30, 315–322.

    PubMed  CAS  Google Scholar 

  20. Kuramoto, H., Kondo, H., and Fujita, T. (1987). Cell Tissue Res. 247, 309–315.

    PubMed  CAS  Google Scholar 

  21. Pelto-Huikko, M. (1989). J. Electr. Microsc. Tech. 12, 364–379.

    CAS  Google Scholar 

  22. Ulrich-Lai, Y. M. and Engeland, W. C. (2000). Neuroendocrinology 71, 107–123.

    PubMed  CAS  Google Scholar 

  23. Edwards, A. V. and Jones, C. T. (1987). J. Physiol. 390, 23–31.

    PubMed  CAS  Google Scholar 

  24. Engeland, W. C. and Gann, D. S. (1989). Neuroendocrinology 50, 124–131.

    PubMed  CAS  Google Scholar 

  25. Walker, C.-D. (1995). Am. J. Physiol. 268, R1281–1288.

    PubMed  CAS  Google Scholar 

  26. Raff, H., Lee, J. L., Widmaier, E. P., Oaks, M. K., and Engeland, W. C. (2004). Endocrinology 145, 79–86.

    PubMed  CAS  Google Scholar 

  27. Ulrich-Lai, Y. M. and Engeland, W. C. (2002). Neuroendocrinology 76, 79–92.

    PubMed  CAS  Google Scholar 

  28. Gallo-Payet, N., Pothier, P., and Isler, H. (1987). Biochem. Cell Biol. 65, 588–592.

    PubMed  CAS  Google Scholar 

  29. Bornstein, S. R., Gonzales-Hernandez, J. A., Ehrhart-Bornstein, M., Adler, G., and Scherbaum, W. A. (1994). J. Clin. Endocrinol. Metab. 78, 225–232.

    PubMed  CAS  Google Scholar 

  30. Ehrhart-Bornstein, M., Hinson, J. P., Bornstein, S. R., Scherbaum, W. A., and Vinson, G. P. (1998). Endocrine Rev. 19, 101–143.

    CAS  Google Scholar 

  31. Veldhuis, J. D. Iranmanesh, A., Lizarralde, G., and Johnson, M. L. (1989). Am. J. Physiol. 257, E6-E14.

    PubMed  CAS  Google Scholar 

  32. Watanabe, K. and Hiroshige, T. (1981). Neuroendocrinology 33, 52–59.

    PubMed  Google Scholar 

  33. Jasper, M. S. and Engeland, W. C. (1991). Am. J. Physiol. 261, R1257-R1268.

    PubMed  CAS  Google Scholar 

  34. Jasper, M. S. and Engeland, W. C. (1994). Neuroendocrinology 59, 97–109.

    PubMed  CAS  Google Scholar 

  35. Jasper, M. S. and Engeland, W. C. (1997). Am. J. Physiol (Endo. Metab.) 273, E363–368.

    CAS  Google Scholar 

  36. Dijkstra, I., Binnekade, R., and Tilders, F. J. H. (1996). Endocrinology 137, 540–547.

    PubMed  CAS  Google Scholar 

  37. Ulrich-Lai, Y. M. and Engeland, W. C. (2005) In: Handbook of stress, immunology and behavior. Steckler, N. K. et al. (ed.). Elsevier Science, Amsterdam.

    Google Scholar 

  38. Kalsbeek, A. and Buijs, R. M. (1992) In: Progress in brain research, 92 ed. Joose, J., Buijs, R. M., and Tilders, F. J. H. (eds.). Elsevier Science Publishers, pp. 321–333.

  39. Buijs, R. M., Wortel, J., Heerikhuize, J. J. v., et al. (1999). Eur. J. Neurosci. 11, 1535–1544.

    PubMed  CAS  Google Scholar 

  40. Niijima, A., Nagai, K., Nagai, N., and Nakagawa, H. (1992). J. Autonomic Nerv. Syst. 40, 155–160.

    CAS  Google Scholar 

  41. McCarty, R., Kvetnansky, R., and Kopin, I. J. (1981). Physiol. Behav. 26, 27–31.

    PubMed  CAS  Google Scholar 

  42. De Boer, S. F. and Van der Gugten, J. (1987). Physiol. Behav. 40, 323–328.

    PubMed  Google Scholar 

  43. Schramm, L. P., Adair, J. R., Stribling, J. M., and Gray, L. P. (1975). Exp. Neurol. 49, 540–53.

    PubMed  CAS  Google Scholar 

  44. Haase, P., Contestabile, A., and Flumerfelt, B. A. (1982). Exp. Neurol. 78, 217–221.

    PubMed  CAS  Google Scholar 

  45. Edwards, A. V. (1982). J. Physiol. 327, 409–419.

    PubMed  CAS  Google Scholar 

  46. Engeland, W. C., Bereiter, D. F., and Gann, D. S. (1986). Am. J. Physiol. 251, R341–348.

    PubMed  CAS  Google Scholar 

  47. Kesse, W. K., Parker, T. L., and Coupland, R. E. (1988). J. Anat. 157, 33–41.

    PubMed  CAS  Google Scholar 

  48. Dagerlind, A., Pelto-Huikko, M., Diez, M., and Hokfelt, T. (1995). Neuroscience 69, 1019–1023.

    PubMed  CAS  Google Scholar 

  49. Afework, M. and Burnstock, G. (1995). Int. J. Dev. Neurosci. 13, 515–521.

    PubMed  CAS  Google Scholar 

  50. Pelto-Huikko, M., Salminen, T., and Hervonen, A. (1985). Histochemistry 82, 377–383.

    PubMed  CAS  Google Scholar 

  51. Swanson, L. W. and Kuypers, H. G. J. M. (1980). J. Comp. Neurol. 194, 555–570.

    PubMed  CAS  Google Scholar 

  52. Sawchenko, P. E., Swanson, L. W., and Vale, W. W. (1984). J. Neurosci. 4, 1118–1129.

    PubMed  CAS  Google Scholar 

  53. Swanson, L. W. and Sawchenko, P.E. (1983). Annu. Rev. Neurosci. 6, 269–324.

    PubMed  CAS  Google Scholar 

  54. Sawchenko, P. E. and Swanson, L. W. (1982). J. Comp. Neurol. 205, 260–272.

    PubMed  CAS  Google Scholar 

  55. Hallbeck, M. and Blomqvist, A. (1999). J. Comp. Neurol. 411, 201–211.

    PubMed  CAS  Google Scholar 

  56. Hallbeck, M., Larhammar, D., and Blomqvist, A. (2001). J. Comp. Neurol. 433, 222–38.

    PubMed  CAS  Google Scholar 

  57. Strack, A. M., Sawyer, W. B., Platt, K. B., and Loewy, A. D. (1989). Brain Res. 491, 274–296.

    PubMed  CAS  Google Scholar 

  58. Strack, A. M. and Loewy, A. D. (1990). J. Neurosci. 10, 2139–2147.

    PubMed  CAS  Google Scholar 

  59. Motawei, K., Pyner, S., Ranson, R. N., Kamel, M., and Coote, J. (1999). Exp. Brain Res. 126, 68–76.

    PubMed  CAS  Google Scholar 

  60. Berk, M. L. and Finkelstein, J. A. (1981). Brain Res. 226, 1–13.

    PubMed  CAS  Google Scholar 

  61. Watts, A. G. and Swanson, L. W. (1987). J. Comp. Neurol. 258, 230–252.

    PubMed  CAS  Google Scholar 

  62. Buijs, R. M., Markman, M., Nunes-Cardoso, B., Hou, Y.-X., and Shinn, S. (1993). J. Comp. Neurol. 335, 42–54.

    PubMed  CAS  Google Scholar 

  63. Inouye, S. T. and Kawamura, H. (1979). Proc. Natl. Acad. Sci. USA 76, 5962–5966.

    PubMed  CAS  Google Scholar 

  64. Meijer, J. H., Schaap, J., Watanabe, K., and Albus, H. (1997). Brain Res. 753, 322–327.

    PubMed  CAS  Google Scholar 

  65. Rusak, B., Robertson, H. A., Wisden, W., and Hunt, S. P. (1990). Science 248, 1237–1240.

    PubMed  CAS  Google Scholar 

  66. Earnest, D. J., Iadarola, M., Yeh, H. H., and Olshowka, J. A. (1990). Exp. Neurol. 109, 353–361.

    PubMed  CAS  Google Scholar 

  67. Nunez, A. A., Bult, A., McElhinny, T. L., and Smale, L. (1999). J. Biol. Rhythms 14, 300–306.

    PubMed  CAS  Google Scholar 

  68. Schwartz, M. D., Nunez, A. A., and Smale, L. (2004). Neuroscience 127, 13–23.

    PubMed  CAS  Google Scholar 

  69. Smale, L., Castleberry, C., and Nunez, A. A. (2001). Brain Res. 899, 101–105.

    PubMed  CAS  Google Scholar 

  70. Choi, S., Wong, L. S., Yamat, C., and Dallman, M. F. (1998). J. Neurosci. 18, 3843–3852.

    PubMed  CAS  Google Scholar 

  71. Grassi-Zucconi, G., Menegazzi, M., Prati, A. C. D., et al. (1993). Eur. J. Neurosci. 5, 1071–1078.

    PubMed  CAS  Google Scholar 

  72. Morton, K. D. R., Kar, L. D. V. d., Brownfield, M. S., and Bethea, C. L. (1989). Neuroendocrinology 50, 73–80.

    PubMed  CAS  Google Scholar 

  73. Ixart, G., Alonso, G., Szafarczyk, A., Malaval, F., Nouguier-Soule, J., and Assenmacher, I. (1982). Neuroendocrinology 35, 270–276.

    PubMed  CAS  Google Scholar 

  74. Watts, A. G., Swanson, L. W., and Sanchez-Watts, G. (1987). J. Comp. Neurol. 258, 204–229.

    PubMed  CAS  Google Scholar 

  75. Teclemariam-Mesbah, R., Kalsbeek, A., Pevet, P., and Buijs, R. M. (1997). Brain Res. 748, 71–76.

    PubMed  CAS  Google Scholar 

  76. Vrang, N., Larsen, P. J., Moller, M., and Mikkelsen, J. D. (1995). J. Comp. Neurol. 353, 585–603.

    PubMed  CAS  Google Scholar 

  77. Abe, K., Kroning, J., Greer, M. A., and Critchlow, V. (1979). Neuroendocrinology 29, 119–131.

    PubMed  CAS  Google Scholar 

  78. Uhl, G. R. and Reppert, S. M. (1986). Science 232, 390–392.

    PubMed  CAS  Google Scholar 

  79. Card, J. P., Fitzpatrick-McElligott, S., Gozes, I., and Baldino, F. (1988). Cell Tissue Res. 252, 307–315.

    PubMed  CAS  Google Scholar 

  80. Albers, H. E., Stopa, E. G., Zoeller, R. T., et al. (1990). Mol. Brain Res. 7, 85–89.

    PubMed  CAS  Google Scholar 

  81. Roland, B. L. and Sawchenko, P. E. (1993). J. Comp. Neurol. 332, 123–143.

    PubMed  CAS  Google Scholar 

  82. Csaki, A., Kocsis, K., Halasz, B., and Kiss, J. (2000). Neuroscience 101, 637–655.

    PubMed  CAS  Google Scholar 

  83. Hermes, M. L. H. J., Coderre, E. M., Buijs, R. M., and Renaud, L. P. (1996). J. Physiol. 496(Pt. 3), 749–757.

    PubMed  CAS  Google Scholar 

  84. Cui, L., Coderre, E., and Renaud, L. P. (2001). Am. J. Physiol. 281, R1283–1289.

    CAS  Google Scholar 

  85. Buijs, R. M., Kalsbeek, A., van der Woude, T. P., van Heerikhuize, J. J., and Shinn, S. (1993). Am. J. Physiol. 264, R1186-R1192.

    PubMed  CAS  Google Scholar 

  86. Kalsbeek, A., Buijs, R. M., van Heerikhuize, J. J., Arts, M., and van der Woude, T. P. (1992). Brain Res. 580, 62–67.

    PubMed  CAS  Google Scholar 

  87. Kalsbeek, A., Vliet, J. v. d., and Buijs, R. M. (1996). J. Neuroendocrinol. 8, 299–307.

    PubMed  CAS  Google Scholar 

  88. Alexander, L. D. and Sander, L. D. (1995). Regul. Peptides 59, 321–333.

    CAS  Google Scholar 

  89. Gilbey, M. P., Coote, J. H., Fleetwood-Walker, S., and Peterson, D. F. (1982). Brain Res. 251, 283–290.

    PubMed  CAS  Google Scholar 

  90. Pyner, S. and Coote, J. H. (2000). Neuroscience 100, 549–556.

    PubMed  CAS  Google Scholar 

  91. Stornetta, R. L., McQuiston, T. J., and Guyenet, P. G. (2004). J. Comp. Neurol. 479, 257–270.

    PubMed  CAS  Google Scholar 

  92. Deuchars, S. A., Milligan, C. J., Stornetta, R. L., and Deuchars, J. (2005). J. Neurosci. 25, 1063–1070.

    PubMed  CAS  Google Scholar 

  93. Gold, P. W., Loriaux, D. L., Roy, A., et al. (1986). N. Engl. J. Med. 314, 1329–1334.

    PubMed  CAS  Google Scholar 

  94. Charlton, B. G. and Ferrier, I. N. (1989). Psych. Med. 19, 331–336.

    CAS  Google Scholar 

  95. O’Brien, J. T., Schweitzer, I., Ames, D., Mastwyk, M., and Colman, P. (1994). Br. J. Psychiatry 165, 650–657.

    PubMed  CAS  Google Scholar 

  96. Amsterdam, J. D., Winkour, A., Abelman, E., Lucki, I., and Rickels, K. (1983). Am. J. Psychiatry 140, 907–909.

    PubMed  CAS  Google Scholar 

  97. Jaeckle, R. S., Kathol, R. G., Lopez, J. F., Meller, W. H., and Krummel, S. J. (1987). Arch. Gen. Psychiatry 44, 233–240.

    PubMed  CAS  Google Scholar 

  98. Nasman, B., Olsson, T., Fagerlund, M., Eriksson, S., Viitanen, M., and Carlstrom, K. (1996). Biol. Psychiatry 39, 311–318.

    PubMed  CAS  Google Scholar 

  99. Pascualy, M., Petrie, E. C., Brodkin, K., Piskind, E. R., Wilkinson, C. W., and Raskind, M. A. (2000). Biol. Psychiatry 48, 247–254.

    PubMed  CAS  Google Scholar 

  100. Kanter, E. D., Wilkinson, C. W., Radant, A. D., et al. (2001). Biol. Psychiatry 50, 238–245.

    PubMed  CAS  Google Scholar 

  101. Yehuda, R. (2002). N. Engl. J. Med. 346, 108–114.

    PubMed  CAS  Google Scholar 

  102. Heim, C., Newport, D. J., Bonsall, R., Miller, A. H., and Nemeroff, C. B. (2001). Am. J. Psychiatry 158, 575–581.

    PubMed  CAS  Google Scholar 

  103. Geracioti, T. D., Baker, D. G., Ekhator, N. N., et al. (2001). Am. J. Psychiatry 158, 1227–1230.

    PubMed  Google Scholar 

  104. Yehuda, R., Siever, L. J., Teicher, M. H., et al. (1998). Biol. Psychiatry 44, 56–63.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Surgery and Neuroscience, Graduate Program in Neuroscience, University of Minnesota, 516 Delaware Street SE, Box 120 UHMC, 55455, Minneapolis, MN

    William C. Engeland PhD & Michelle M. Arnhold

Authors
  1. William C. Engeland PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michelle M. Arnhold
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to William C. Engeland PhD.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Engeland, W.C., Arnhold, M.M. Neural circuitry in the regulation of adrenal corticosterone rhythmicity. Endocr 28, 325–331 (2005). https://doi.org/10.1385/ENDO:28:3:325

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/ENDO:28:3:325

Key Words

Search

Navigation