Advertisement

Neuronal Circuits and Neuroendocrine Responses Involved in Dehydration Induced by Water Restriction/Deprivation

  • Zheng-Hua Zhu
  • Bai-Ren Wang
  • James S. McTaggart
  • Li-Ze Xiong
Chapter

Abstract

Body fluid balance is essential for survival. Dehydration caused by water restriction or deprivation induces a loss of intracellular and extracellular fluid (ECF) – decreasing cell and plasma volume – and increases osmolarity. This elevates serum sodium concentrations. Dehydration is also accompanied by thirst and increased salt appetite as well as behavioral responses, such as increased water-seeking and water intake, and ingestion of salt-containing food/fluid in an effort to maintain fluid balance. These changes are mediated in part by the action of the autonomic nervous system and the renin–angiotensin system, but nuclei in the brain also play a crucial role, which is the focus of this review.
  1. 1.

    A variety of brain regions are involved in sensing alterations of body fluid volume and osmolarity. Circumventricular organs (CVOs) including the subfornical organ (SFO), the organum vasculosum laminae terminalis (OVLT), the median preoptic nucleus (MnPO), and the area postrema (AP) contain copious osmoreceptors and are known as the “sensory complex.” In addition, neurons in the nucleus tractus solitarius (NTS) relay peripheral signals to other areas of the brain, and neurons in the lateral parabrachial nucleus (LPB) integrate information from the hypothalamo-neurohypophyseal system (HNS) or the AP/NTS and act to modulate motor behavior.

     
  2. 2.

    Neurons in the supraoptic nucleus (SON) and hypothalamic paraventricular nucleus (PVN), which receive signals from the intrinsic osmoreceptors and the CVOs as well as NTS, release oxytocin (OT) and arginine vasopressin (AVP) into the general circulation to modulate water retention and natriuresis. These processes are also modulated by classic neurotransmitters such as norepinephrine (NE), glutamate, γ-aminobutyric acid (GABA), nitric oxide (NO), and many other neuropeptide transmitters such as angiotensin II (AngII), corticotrophin-releasing hormone (CRH), apelin, galanin, estrogens (Es), obestatin, orexin, and neuropeptide Y (NPY).

     
  3. 3.

    In addition to OT, AVP and some other known genes being up- or downregulated, several novel genes are thought to be involved in neuronal responses to dehydration.

     
  4. 4.

    Glia may also influence water and salt balance via modulation of sodium-level-sensitive sodium channels (Nax), aquaporin-4 water channels (AQP4), and secretion of taurine in CVOs and the HNS.

     
Further investigation of dehydration-induced central neuronal plasticity and remodeling may reveal new drug targets for the treatment of clinical disorders that result in perturbation of water/salt balance.

Keywords

Atrial Natriuretic Peptide Water Deprivation Nucleus Tractus Solitarius Area Postrema Orexin Neuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ACTH

Adrenocorticotropic hormone

AngII

Angiotensin II

AP

Area postrema

AQP4

Aquaporin-4

AV3V

Anteroventral third ventricle area

AVP

Arginine vasopressin

avPVN

Anteroventral part of PVN

BNST

Bed nuclei of the stria terminalis

CeA

Central amygdaloid nucleus

CNS

Central nervous system

CRH

Corticotropin releasing hormone

CVOs

Circumventricular organs

E

Estrogen

ECF

Extracellular fluid

ER

Estrogen receptor

Fos-LIR

Fos-like immunoreactivity

GABA

γ-aminobutyric acid

GFAP

Glial fibrillary acidic protein

HNS

Hypothalamo-neurohypophyseal system

ICF

Intracellular fluid

LPB

Lateral parabrachial nucleus

LSV

Ventrolateral septum

MCNs

Magnocellular neurosecretory cells

MeA

Medial amygdaloid nucleus

MnPO

Median preoptic nucleus

NE

Norepinephrine

NIL

Neurointermediate lobe

NO

Nitric oxide

NTS

Nucleus tractus solitarius

OT

Oxytocin

OVLT

Organum vasculosum of the lamina terminalis

PVN

Hypothalamic paraventricular nucleus

SFO

Subfornical organ

SON

Supraoptic nucleus

References

  1. Albrecht J, Schousboe A. Neurochem Res. 2005;30:1615–21.PubMedCrossRefGoogle Scholar
  2. Antunes-Rodrigues J, de Castro M, Elias LL, Valenca MM, McCann SM. Physiol Rev. 2004;84:169–208.PubMedCrossRefGoogle Scholar
  3. Arima H, Aguilera G. J Neuroendocrinol.2000;12:833–42.PubMedCrossRefGoogle Scholar
  4. Arnhold MM, Wotus C, Engeland WC. Exp Neurol. 2007;206:126–36.PubMedCrossRefGoogle Scholar
  5. Bourque CW, Oliet SH. Annu Rev Physiol. 1997;59:601–19.PubMedCrossRefGoogle Scholar
  6. Bundzikova J, Pirnik Z, Zelena D, Mikkelsen JD, Kiss A. Cell Mol Neurobiol. 2008;28:1033–47.PubMedCrossRefGoogle Scholar
  7. Chae HE, Heideman PD. Brain Res. 1998;791:1–10.PubMedCrossRefGoogle Scholar
  8. Ciosek J, Cisowska A. J Physiol Pharmacol. 2003;54:625–41.PubMedGoogle Scholar
  9. da Silveira LT, Junta CM, Monesi N, de Oliveira-Pelegrin GR, Passos GA, Rocha MJ. Cell Mol Neurobiol. 2007;27:575–84.PubMedCrossRefGoogle Scholar
  10. Di S, Tasker JG. Endocrinology 2004;145:5141–9.PubMedCrossRefGoogle Scholar
  11. Garcia-Segura LM, McCarthy MM. Endocrinology 2004;145:1082–6.PubMedCrossRefGoogle Scholar
  12. Ghorbel MT, Sharman G, Hindmarch C, Becker KG, Barrett T, Murphy D. Physiol Genomics. 2006;24:163–72.PubMedGoogle Scholar
  13. Gillard ER, Coburn CG, de Leon A, Snissarenko EP, Bauce LG, Pittman QJ, Hou B, Currás-Collazo MC. Endocrinology 2007;148:479–89.PubMedCrossRefGoogle Scholar
  14. Goldin AL, Barchi RL, Caldwell JH, Hofmann F, Howe JR, Hunter JC, Kallen RG, Mandel G, Meisler MH, Netter YB, Noda M, Tamkun MM, Waxman SG, Wood JN, Catterall WA. Neuron 2000;28:365–8.PubMedCrossRefGoogle Scholar
  15. Gouraud SS, Heesom K, Yao ST, Qiu J, Paton JF, Murphy D. Endocrinology 2007;148:3041–52.PubMedCrossRefGoogle Scholar
  16. Hawrylak N, Fleming JC, Salm AK. Glia 1998;22:260–71.PubMedCrossRefGoogle Scholar
  17. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE. Front Neuroendocrin 2003;24:151–80.CrossRefGoogle Scholar
  18. Hindmarch C, Yao S, Beighton G, Paton J, Murphy D. Proc Natl Acad Sci U S A. 2006;103:1609–14.PubMedCrossRefGoogle Scholar
  19. Hindmarch C, Fry M, Yao ST, Smith PM, Murphy D, Ferguson AV. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1914–20.PubMedCrossRefGoogle Scholar
  20. Hiyama TY, Watanabe E, Ono K, Inenaga K, Tamkun MM, Yoshida S, Noda M. Nat Neurosci. 2002;5:511–2.PubMedCrossRefGoogle Scholar
  21. Hiyama TY, Watanabe E, Okado H, Noda M. J Neurosci. 2004;24:9276–81.PubMedCrossRefGoogle Scholar
  22. Honda K, Negoro H, Dyball RE, Higuchi T, Takano S. J Physiol. 1990;431:225–41.PubMedGoogle Scholar
  23. Hussy N, Deleuze C, Desarménien MG, Moos FC. Prog Neurobiol. 2000;62:113–34.PubMedCrossRefGoogle Scholar
  24. Johnson AK, Thunhorst RL. Front Neuroendocrin. 1997;18:292–353.CrossRefGoogle Scholar
  25. Kadekaro M. Braz J Med Biol Res. 2004;37:441–50.PubMedCrossRefGoogle Scholar
  26. Kadekaro M, Su G, Chu R, Lei Y, Li J, Fang L. Neurosci Lett. 2006;404:50–5.PubMedCrossRefGoogle Scholar
  27. Kozoriz MG, Kuzmiski JB, Hirasawa M, Pittman QJ. J Neurophysiol. 2006;96:154–64.PubMedCrossRefGoogle Scholar
  28. Lang R, Gundlach AL, Kofler B. Pharmacol Ther. 2007;115:177–207.PubMedCrossRefGoogle Scholar
  29. Larsen PJ, Mikkelsen JD, Jessop DS, Lightman SL, Chowdrey HS. J Neurosci. 1993;13:1138–47.PubMedGoogle Scholar
  30. Lauand F, Ruginsk SG, Rodrigues HLP, Reis WL, De Castro M, Elias LLK, Antunes-Rodrigues J. Neuroscience 2007;147:247–57.PubMedCrossRefGoogle Scholar
  31. Llorens-Cortes C, Moos F. Prog Brain Res. 2008;170:559–70.PubMedCrossRefGoogle Scholar
  32. McKinley MJ, Hards DK, Oldfield BJ. Brain Res. 1994;653:305–14.PubMedCrossRefGoogle Scholar
  33. Miyata S, Takamatsu H, Maekawa S, Matsumoto N, Watanabe K, Kiyohara T, Hatton GI. J Comp Neurol. 2001;434:413–27.PubMedCrossRefGoogle Scholar
  34. Morien A, Garrard L, Rowland NE. Brain Res. 1999;816:1–7.PubMedCrossRefGoogle Scholar
  35. Murugaiyan P, Salm AK. Glia 1995;15:65–76.PubMedCrossRefGoogle Scholar
  36. Newman EA, Volterra A. Glia 2004;47:207–8.PubMedCrossRefGoogle Scholar
  37. Nielsen S, Nagelhus EA, Amirty-Moghaddam M, Bourque C, Agre P, Ottersen OP. J Neurosci. 1997;17:171–80.PubMedGoogle Scholar
  38. Noda M. Exp Physiol. 2007;92:513–22.PubMedCrossRefGoogle Scholar
  39. Noda M, Hiyama TY. Chem Senses. 2005;30:i44–5.PubMedCrossRefGoogle Scholar
  40. Pacak K, Palkovits M. Endocr Rev. 2001;22:502–48.PubMedCrossRefGoogle Scholar
  41. Rawland NE. Neurosci Biobehav Rev. 1998;23:49–63.CrossRefGoogle Scholar
  42. Reaux A, De Mota N, Skultetyova I, Lenkei Z, El Messari S, Gallatz K, Corvol P, Palkovits M, Llorens-Corte’s C. J Neurochem. 2001;77:1085–96.PubMedCrossRefGoogle Scholar
  43. Reaux-Le Goazigo A, Morinville A, Burlet A, Llorens-Corte’s C, Beaudet A. Endocrinology. 2004;145:4392–400.PubMedCrossRefGoogle Scholar
  44. Samson WK, White MM, Price CP, Ferguson AV. Am J Physiol. 2007;292:R637–43.Google Scholar
  45. Samson WK, Yosten GL, Chang JK, Ferguson AV, White MM. J Endocrinol. 2008;196:559–64.PubMedCrossRefGoogle Scholar
  46. Sharman G, Ghorbel M, Leroux M, Beaucourt S, Wong LF, Murphy D. Prog Biophys Mol Biol. 2004;84:151–82.PubMedCrossRefGoogle Scholar
  47. Simard M, Nedergaard M. Neuroscience 2004;129:877–96.PubMedCrossRefGoogle Scholar
  48. Sladek CD, Somponpun SJ. Front Neuroendocrin. 2008;29:114–27.CrossRefGoogle Scholar
  49. Tait MJ, Saadoun S, Bell BA, Papadopoulos MC. Trends Neurosci. 2008;31:37–43.PubMedCrossRefGoogle Scholar
  50. Theodosis DT, El Majdoubi M, Pierre K, Poulain DA. Cell Mol Neurobiol. 1998;18:285–98.PubMedCrossRefGoogle Scholar
  51. Tsunematsu T, Fu LY, Yamanaka A, Ichiki K, Tanoue A, Sakurai T, van den Pol AN. J Neurosci. 2008;28:228–38.PubMedCrossRefGoogle Scholar
  52. Ueta Y, Yamashita H, Kawata M, Koizumi K. Brain Res. 1995;677:221–8.PubMedCrossRefGoogle Scholar
  53. Urban JH, Leitermann RJ, DeJoseph MR, Somponpun SJ, Wolak ML, Sladek CD. Endocrinology 2006;147:4122–31.PubMedCrossRefGoogle Scholar
  54. Van de Kar LD, Blair ML. Front Neuroendocrin. 1999;20:1–48.CrossRefGoogle Scholar
  55. Virard I, Gubkina O, Alfonsi F, Durbec P. Neuroscience 2008;151:82–91.PubMedCrossRefGoogle Scholar
  56. Watanabe E, Fujikawa A, Matsunaga H, Yasoshima Y, Sako N, Yamamoto T, Saegusa C, Noda M. J Neurosci. 2000;20:7743–51.PubMedGoogle Scholar
  57. Watanabe E, Hiyama TY, Shimizu H, Kodama R, Hayashi N, Miyata S, Yanagawa Y, Obata K, Noda M. Am J Physiol Regul Integr Comp Physiol. 2006;290:R568–76.PubMedCrossRefGoogle Scholar
  58. Watts AG. Annu Rev Neurosci. 2001;24:357–84.PubMedCrossRefGoogle Scholar
  59. Wells T. Mol Cell Endocrinol. 1998;136:103–7.PubMedCrossRefGoogle Scholar
  60. Xiong JJ, Hatton GI. Brain Res. 1996;719:143–53.PubMedCrossRefGoogle Scholar
  61. Zhang Z, Bourque CW. Nat Neurosci. 2003;6:1021–2.PubMedCrossRefGoogle Scholar
  62. Zhu ZH, Wang BR, Tan QR, Duan XL, Kuang F, Xu Z, Ju G. Neurosci Bull. 2006;22:144–50.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Zheng-Hua Zhu
  • Bai-Ren Wang
  • James S. McTaggart
  • Li-Ze Xiong
    • 1
  1. 1.Department of Anesthesiology, Xijing HospitalFourth Military Medical UniversityXi’anChina

Personalised recommendations