Skip to main content
Log in

Hibernation-related changes in the immunoreactivity of neuropeptide systems in the suprachiasmatic nucleus of the ground squirrel, Spermophilus richardsonii

With reference to observations in the hedgehog, Erinaceus europaeus

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The pattern of distribution and reactivity of the neuropeptides vasopressin (AVP), vasoactive intestinal peptide (VIP), neuropeptide Y (NPY), substance P (SP), and thyrotropin-releasing hormone (TRH) were studied in the suprachiasmatic nucleus (NSC) of 20 Richardson's ground squirrels (and 7 European hedgehogs) of both sexes during hibernation and euthermia. The total area of immunostained structures revealed by application of the individual immunocytochemical techniques was measured by means of computer-aided image analysis. In both species, elements of all peptide systems examined were related to particular subdivisions of the NSC. The pattern of immunoreactivity was strongly correlated with the physiological stage of hibernation or euthermia both in ground squirrels and hedgehogs. The immunoreactivities to AVP and SP increased in area during hibernation (AVP: 25%; SP: 25%), whereas the respective area immunoreactive to NPY and VIP decreased (NPY: 45%; VIP: 100%) in comparison to nonhibernating controls. The TRH-immunoreactive nerve fibers were rare and rather scattered; thus, the quantitative procedure was not applicable for this immunoreaction.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AVP :

argnine vasopressin

NPY :

neuropeptide Y

NSC :

suprachiasmatic nucleus

SP :

substance P

TRH :

thyrotropinreleasing hormone

VIP :

vasoactive intestinal peptide

References

  • Albers HE, Stopa EG, Zoeller RT, Kauer JS, King JC, Fink JS, Mobtaker H, Wolfe H (1990) Day-night variation in prepro vasoactive intestinal peptide/peptide histidine isoleucine mRNA within the rat suprachiasmatic nucleus. Mol Brain Res 7:85–89

    Google Scholar 

  • Canguilhem B, Kempf E, Mack G, Schmitt P (1977) Regional studies of brain serotonin and norepinephrine in the hibernating, awaking or active European hamster, Cricetus cricetus, during winter. Comp Biochem Physiol 57C:175–179

    Google Scholar 

  • Card JP, Moore RY (1984) The suprachiasmatic nucleus of the golden hamster: immunohistochemical analysis of cell and fiber distribution. Neuroscience 13:415–431

    Google Scholar 

  • Cassone VM, Moore RY (1987) Retinohypothalamic projection and suprachiasmatic nucleus of the house sparrow, Passer domesticus. J Comp Neurol 266:171–182

    Google Scholar 

  • Dark J, Pickard GE, Zucker I (1985) Persistence of circannual rhythms in ground squirrels with lesions of the suprachiasmatic nucleus. Brain Res 332:201–207

    Google Scholar 

  • Earnest DJ, Sladek CD (1986) Circadian rhythms of vasopressin release from individual rat suprachiasmatic explants in vitro. Brain Res 382:129–133

    Google Scholar 

  • Gillette MU, Prosser RA (1988) Circadian rhythm of the rat suprachiasmatic brain slice is rapidly reset by daytime application of cAMP analogs. Brain Res 474:348–352

    Google Scholar 

  • Güldner FH (1976) Synaptology of the rat suprachiasmatic nucleus. Cell Tissue Res 165:509–544

    Google Scholar 

  • Guy J, Bosler O, Dusticier G, Pelletier G, Calas A (1987) Morphological correlates of serotonin — neuropeptide Y interactions in the rat suprachiasmatic nucleus: Combined radioautographic and immunocytochemical data. Cell Tissue Res 250:657–662

    Google Scholar 

  • Hermes MLHJ, Buijs RM, Masson-Pévet M, Woude TP van der, Pévet P, Brenklé R, Kirsch R (1989) Central vasopressin infusion prevents hibernation in the European hamster (Cricetus cricetus). Proc Natl Acad Sci USA 86:6408–6411

    Google Scholar 

  • Hery M, Barrit MC, Faudon M, Hery F (1986) Effect of vasoactive intestinal peptide on serotonin metabolism in the suprachiasmatic area of the rat: mechanism of action. Peptides 7:183–188

    Google Scholar 

  • Hökfelt T, Millhorn D, Seroogy K, Tsuruo Y, Ceccatelli S, Lindh B, Meister B, Melander I, Schalling M, Bartfai T, Terenius L (1987) Coexistence of peptides with classical neurotransmitters. Experientia 43:768–780

    Google Scholar 

  • Kilduff TS, Sharp FR, Heller HC (1982) 14C 2-deoxyglucose uptake in ground squirrel brain during hibernation. J Neurosci 2:143–157

    Google Scholar 

  • Kilduff TS, Redeke CD, Heller HC (1986) Neural activity during mammalian hibernation. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold. Physiological and biochemical adaptations. Elsevier, New York, pp 215–223

    Google Scholar 

  • Klüver H, Barrera E (1953) A method for the combined staining of cells and fibers in the nervous system. J Neuropathol Exp Neurol 12:400–403

    Google Scholar 

  • Meijer JH, Rusak B, Harrington ME (1989) Photically responsive neurons in the hypothalamus of a diurnal ground squirrel. Brain Res 501:315–323

    Google Scholar 

  • Moore RY (1973) Retinohypothalamic projection in mammals: a comparative study. Brain Res 49:403–419

    Google Scholar 

  • Moore RY (1979) The retinohypothalamic tract, suprachiasmatic nucleus and central neural mechanisms of circadian rhythms regulation. In: Suda H, Hayashi O, Nagakawa H (eds) Biological rhythms and their central mechanisms. Elsevier, Amsterdam, pp 343–354

    Google Scholar 

  • Moore RY (1982) The suprachiasmatic nucleus and the organization of a circadian system. TINS 404–407

  • Newman G (1990) SCN metabolic activity in vitro. In: Klein DC, Moore RY, Reppert SM (eds) Suprachiasmatic nucleus: the mind's clock. Oxford University Press, New York (in press)

    Google Scholar 

  • Newman GC, Hospod FE (1986) Rhythm of suprachiasmatic nucleus 2-deoxyglucose uptake in vitro. Brain Res 381:345–350

    Google Scholar 

  • Norgren RB, Silver R (1989) Distribution of vasoactive intestinal peptide-like and neurophysin-like immunoreactive neurons and acetylcholinesterase staining in the ring dove hypothalamus with emphasis on the question of an avian suprachiasmatic nucleus. Cell Tissue Res 259:331–339

    Google Scholar 

  • Nürnberger F (1983) Der Hypothalamus des Igels (Erinaceus eruopaeus L.) unter besonderer Berücksichtigung des Winterschlafes. Cytoarchitektonische und immunocytochemische Studien. Dissertation, Marburg

  • Nürnberger F, Blähser S, Merker G (1982) Reactivity pattern of vasopressin neurons in long-term hibernations. Pflügers Arch 392 [Suppl]:R31

  • Nürnberger F, Rørstad OP, Lederis K (1985) The hypothalamo-neurohypophysial system and hibernation in the ground squirrel Spermophilus richardsonii. In: Kobayashi H, Bern HA, Urano A (eds) Neurosecretion and the biology of neuropeptides. Japan Sci Soc Press, Tokyo/Springer, Berlin Heidelberg New York, pp 518–520

    Google Scholar 

  • Nürnberger F, Lederis K, Rørstad OP (1986) Effect of hibernation on somatostatin-like immunoreactivity in the brain of the ground squirrel (Spermophilus richardsonii) and European hedgehog (Erinaceus europaeus). Cell Tissue Res 243:263–271

    Google Scholar 

  • Nürnberger F, Schindler CU, Kriete A (1989) The serotonin-immunoreactive system of the suprachiasmatic nucleus in the hibernating ground squirrel, Spermophilus richardsonii. Cell Tissue Res 256:593–599

    Google Scholar 

  • Pickard GE (1985) Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suprachiasmatic nucleus and the intergeniculate leaflet of the thalamus. Neurosci Lett 55:211–217

    Google Scholar 

  • Pol AN van den (1990) Intrinsic organization of the suprachiasmatic nucleus: neurochemical and cytological characteristics. In: Klein DC, Moore RY, Reppert SM (eds) Suprachiasmatic nucleus: the mind's clock. Oxford University Press, New York (in press)

    Google Scholar 

  • Pol AN van den, Tsujimoto K (1985) Neutrotransmitters of the hypothalamic suprachiasmatic nucleus: Immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15:1049–1086

    Google Scholar 

  • Pol AN van den, Gorcs T (1986) Synaptic relationships between neurons containing vasopressin, gastrin-releasing peptide, vasoactive intestinal polypeptide, and glutamate decarboxylase immunoreactivity in the suprachiasmatic nucleus: dual ultrastructural immunocytochemistry with gold-substituted silver peroxydase. J Comp Neurol 252:507–521

    Google Scholar 

  • Popova NK, Voitenko NN (1981) Brain serotonin metabolism in hibernation. Pharmacol Biochem Behav 14:773–777

    Google Scholar 

  • Reppert SM, Uhl GR (1988) Vasopressin messenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: appearance and circadian regulation during development. Endocrinology 120:2483–2487

    Google Scholar 

  • Reuss S, Hurlbut EC, Speh JC, Moore RY (1989) Immunohistochemical evidence for the presence of neuropeptides in the hypothalamic suprachiasmatic nucleus of ground squirrels. Anat Rec 225:341–346

    Google Scholar 

  • Scammell TE, Schwartz WJ, Smith CB (1989) No evidence for a circadian rhythm of protein synthesis in the rat suprachiasmatic nuclei. Brain Res 494:155–158

    Google Scholar 

  • Schindler CU, Kriete A, Nürnberger F (1989) Aminerge und peptiderge Systeme im Nucleus suprachiasmaticus des Winterschläfers Spermophilus richardsonii. Anat Anz 80:90–91

    Google Scholar 

  • Schwartz WJ, Reppert SM (1985) Neural regulation of the circadian vasopressin rhythm in cerebrospinal fluid: a pre-eminent role for the suprachiasmatic nuclei. J Neurosci 5:2771–2778

    Google Scholar 

  • Schwartz WJ (1990) SCN metabolic activity in vivo. In: Klein DC, Moore RY, Reppert SM (eds) Suprachiasmatic nucleus: the mind's clock. Oxford University Press, New York (in press)

    Google Scholar 

  • Sternberger LA, Hardy PH, Cuculis JJ, Meyer HG (1970) The unlabeled antibody enzyme method of immunocytochemistry. Preparations and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem 18:315–333

    Google Scholar 

  • Stopa EG, King JC, Lydic R, Schoene WC (1984) Human brain contains vasopressin and vasoactive intestinal polypeptide neuronal subpopulations in the suprachiasmatic region. Brain Res 297:159–163

    Google Scholar 

  • Ueda S, Kawata M, Sano Y (1986) Identification of neuropeptide Y immunoreactivity in the suprachiasmatic nucleus and the lateral geniculate nucleus of some mammals. Neurosci Lett 68:7–10

    Google Scholar 

  • Vanecek J, Pavlik A, Illnerova H (1987) Hypothalamic melatonin receptor sites revealed by autoradiography. Brain Res 435:359–362

    Google Scholar 

  • Wang LCH (1989) Animal adaptation to cold. Springer, Berlin Heidelberg, New York

    Google Scholar 

  • Zucker I, Dark J, Lee TM (1990) Involvement of the suprachiasmatic nuclei in generation and entrainment of annual rhythms in mammals. In: Klein DC, Moore RY, Reppert SM (eds) Suprachiasmatic nucleus: the mind's clock. Oxford University Press, New York (in press)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schindler, C.U., Nürnberger, F. Hibernation-related changes in the immunoreactivity of neuropeptide systems in the suprachiasmatic nucleus of the ground squirrel, Spermophilus richardsonii . Cell Tissue Res 262, 293–300 (1990). https://doi.org/10.1007/BF00309884

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00309884

Key words

Navigation