Skip to main content
SpringerLink
Log in

Tyrosine hydroxylase- and neuropeptide Y-immunoreactive nerve fibers in the pineal complex of untreated rats and rats following removal of the superior cervical ganglia

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

Summary

The distribution of tyrosine hydroxylase (TH)- and neuropeptide Y (NPY)-immunoreactive(IR) nerve fibers in the pineal complex was investigated in untreated rats and rats following bilateral removal of the superior cervical ganglia. In normal animals, a large number of TH- and NPY-IR nerve fibers were present in the pineal capsule, the perivascular spaces, and intraparenchymally between the pinealocytes throughout the superficial pineal and deep pineal gland. A small number of TH-IR and NPY-IR nerve fibers were found in the posterior and habenular commissures, a few fibers penetrating from the commissures into the deep pineal gland. To elucidate the origin of these fibers, the superior cervical ganglion was removed bilaterally in 10 animals, and the pineal complex was examined immunohistochemically. Two weeks after the ganglionectomy, the TH-IR and NPY-IR nerve fibers in the superficial pineal gland had almost completely disappeared. On the other hand, in the deep pineal and the pineal stalk, the TH-IR and NPY-IR fibers were still present after ganglionectomy. These data show that the deep pineal gland and the pineal stalk possess an extrasympathetic innervation by TH-IR and NPY-IR fibers. It is suggested that the extrasympathetic TH-IR and NPY-IR nerve fibers innervating the deep pineal and the pineal stalk originate from the brain.

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

  • Adrian TE, Allen JM, Bloom SR, Ghatai MA, Rosset MN, Roberts GW, Crow TJ, Tatemoto K, Polak JM (1983) Neuropeptide Y distribution in human brain. Nature 306:584–586

    Google Scholar 

  • Albers HE, Ferris CF (1984) Neuropeptide Y: role in the light-dark cycle entrainment of hamster circadian rhythms. Neurosci Lett 50:163–168

    Google Scholar 

  • Allen JM, Bloom SR (1986) Neuropeptide Y: a putative neurotransmitter. Neurochem Int 8:1–8

    Google Scholar 

  • Card JP, Moore RY (1989) Organizatio of lateral geniculate-hypothalamic connections in the rat. J Comp Neurol 284:135–147

    Google Scholar 

  • Chronwall BM, DiMaggio DA, Massaru VJ, Pickel VM, Ruggeriero DA, O'Donohue TL (1985) The anatomy of neuropeptide Y containing neurons in the rat brain. Neuroscience 15:1159–1181

    Google Scholar 

  • Colmers WF, Pittman QJ (1990) Presynaptic inhibition by neuropeptide Y and baclofen in hippocampus: intensitivity to pertussis toxin treatment. Brain Res 498:99–104

    Google Scholar 

  • Colmers WF, Lukowiak K, Pittman QJ (1985) Neuropeptide Y reduces orthodromically evoked population spike in rat hippocampal CA1 by a possibly presynaptic mechanism. Brain Res 346:404–408

    Google Scholar 

  • Edvinsson L, Ekblad E, Håkanson R, Wahlestedt C (1984) Neuropeptide Y potentiates the effect of various vasoconstrictor agents on rabbit blood vessels. Br J Pharmacol 83:519–525

    Google Scholar 

  • Everitt BJ, Hökfelt T, Terenius L, Tatemoto K, Mutt V, Goldstein M (1984) Differential co-existence of neuroeptide Y (NPY)-like immunoreactivity with catecholamines in the central nervous system of rat. Neuroscience 11:443–462

    Google Scholar 

  • Gibbins IL, Morris JL (1987) Coexistence of neuropeptides in sympathetic, cranial autonomic and sensory neurons innervating the iris of the guinea pig. J Auton Nerv Syst 21:67–82

    Google Scholar 

  • Haas HL, Hermann A, Greene RW, Chan-Palay V (1987) Action and location of neuropeptide tyrosine(Y) on hippocampal neurons of the rat in slice preparations. J Comp Neurol 257:208–215

    Google Scholar 

  • Hamassaki DE, Britto LRG (1990) Thalamic origin of neuropeptide Y innervation of the accessory optic nucleus of the pigeon (Columba livia). Visual Neurosci 5:249–259

    Google Scholar 

  • Harrington ME, Nance DM, Rusak B (1990) Double-labeling of neuropeptide Y-immunoreactive neurons which project from the geniculate to the suprachiasmatic nuclei. Brain Res 410:275–282

    Google Scholar 

  • Kappers JA (1960) The development, topographical relations and innervation of the epiphysis cerebri in the albino rat. Z Zellforsch 52:163–215

    Google Scholar 

  • Korf HW, Møller M (1985) The central innervation of the mammalian pineal organ. In: Mess B, Ruzsas CS, Tima L, Pévet P (eds) The pineal gland. Akadémiai Kiadó, Budapest, pp 47–69

    Google Scholar 

  • Kuwayama Y, Emson PC, Stone RA (1988) Pterygopalatine ganglion cells contain neuropeptide Y. Brain Res 446:219–224

    Google Scholar 

  • Larhammar D, Ericsson A, Persson H (1987) Structure and expression of the rat neuropeptide Y gene. Proc Natl Acad Sci USA 84:2068–2072

    Google Scholar 

  • Leblanc GG, Trimmer BA, Landis SC (1987) Neuropeptide Y-like immunoreactivity in rat cranial parasympathetic neurons: coexistence with vasoactive intestinal peptide and choline acetyltransferase. Proc Natl Acad Sci USA 84:3511–3515

    Google Scholar 

  • Leger L, Charnay Y, Danger JM, Vaudry H, Pelletier G, Dubois P-M, Jouvet M (1987) Mapping of neuropeptide Y-like immuno-reactivity in the feline hypothalamus and hypophysis. J Comp Neurol 255:238–292

    Google Scholar 

  • Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom S, Goldstein M (1982) Neuropeptide Y(NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol Scand 116:477–480

    Google Scholar 

  • Martin CH, Meissl H (1990) Characterization of the light response in the pineal gland of intact and sympathectomized rats. J Neural Transm 79:81–91

    Google Scholar 

  • Mikkelsen JD (1990) Projections from the lateral geniculate nucleus to the hypothalamus of the Mongolian gerbil (Meriones unguiculatus). An anterograde and retrograde tracing study. J Comp Neurol 299:493–508

    Google Scholar 

  • Mikkelsen JD, Møller M (1990) A direct neural projection from the intergeniculate leaflet of the lateral geniculate nucleus to the deep pineal gland of the rat, demonstrated with Phaseolus vulgaris leucoagglutinin. Brain Res 520:342–346

    Google Scholar 

  • Mikkelsen JD, O'Hare MMT (1991) An immunohistochemical and chromatographic analysis of the distribution and processing of proneuropeptide Y in the rat suprachiasmatic nucleus. Peptides 12:177–185

    Google Scholar 

  • Mikkelsen JD, Cozzi B, Møller M (1991) Efferent projections from the lateral geniculate body to the pineal complex of the Mongolian gerbil (Meriones unguiculatus). Cell Tissue Res 264:95–102

    Google Scholar 

  • Minth CD, Bloom SR, Polak JM, Dixon JE (1984) Cloning, characterization and DNA sequence of a human cDNA encoding neuropeptide tyrosine. Proc Natl Acad Sci USA 81:4577–4581

    Google Scholar 

  • Møller M, Korf HW (1983) The origin of central pinealopetal nerve fibers in the Mongolian gerbil as demonstrated by the retrograde transport of horseradish peroxidase. Cell Tissue Res 230:273–278

    Google Scholar 

  • Møller M, Korf HW (1987) Nervous connections between the brain and the pineal gland of the golden hamster (Mesocricetus auratus). A horseradish peroxidase study. Cell Tissue Res 247:145–153

    Google Scholar 

  • Møller M, Cozzi B, Schröder H, Mikkelsen JD (1987) The peptidergic innervation of the mammalian pineal gland. In: Trentini GP, Gaetani C De, Pévet P (eds) Fundamentals and clinics in pineal research. Serono Symposia Publication no 44. Raven Press, New York, pp 71–77

    Google Scholar 

  • Møller M, Mikkelsen JD, Martinet L (1990) Innervation of the mink pineal with neuropeptide Y (NPY)-containing nerve fibers. An experimental immunohistochemical study. Cell Tissue Res 261:477–483

    Google Scholar 

  • Morgan PJ, Williams LM, Lawson W, Riddoch G (1988a) Stimulation of melatonin synthesis in ovine pineals in vitro. J Neurochem 50:75–81

    Google Scholar 

  • Morgan PJ, Williams LM, Lawson W, Riddoch G (1988b) Adrenergic and VIP stimulation of cyclic AMP accumulation in ovine pineal. Brain Res 447:279–286

    Google Scholar 

  • Nagatsu T, Levitt M, Udenfriend S (1964) Tyrosine hydroxylase: The initial step in norepinephrine biosynthesis. J Biol Chem 239:2910–2917

    Google Scholar 

  • Olcese J (1990) Neuropeptide Y-mediated inhibition of adrenergicstimulated melatonin synthesis in rat pinealocyte cultures. Proc 5th Coll EPSG, Guildford, p 72

  • Pelletier G, Guy J, Allen Y, Polak JM (1984) Electron microscope immunocytochemical localization of neuropeptide Y in the rat brain. Neuropeptides 4:319–324

    Google Scholar 

  • Potter EK, Mitchell L, McCloskey MJD, Tseng A, Amanda E, Goodman E, Shine J, McCloskey DI (1989) Pre- and postjunctional actions of neuropeptide Y and related peptides. Regul Pept 25:167–177

    Google Scholar 

  • Reuss S, Schröder H (1987) Neuropeptide Y effects on pineal melatonin synthesis in the rat. Neurosci Lett 74:158–162

    Google Scholar 

  • Rønnekleiv OK, Møller M (1979) Brain-pineal nervous connections in the rat: an ultrastructure study following habenular lesion. Exp Brain Res 37:551–562

    Google Scholar 

  • Sawchenko PE, Swanson LW, Grzanne R, Howe PCR, Bloom SR, Polak JM (1985) Colocalization of neuropeptide Y immunoreactivity in the brainstem catecholaminergic neurons that project to the paraventricular nucleus of the hypothalamus. J Comp Neurol 241:138–153

    Google Scholar 

  • Schon F, Allen JM, Yeats JC, Allen YS, Ballesta J, Polak JM, Kelly JS, Bloom SR (1985) Neuropeptide Y innervation of the rodent pineal gland and cerebral vessels. Neurosci Lett 57:65–71

    Google Scholar 

  • Schröder H (1986) Neuropeptide Y (NPY)-like immunoreactivity in peripheral and central fibres of the golden hamster (Mesocricetus auratus) with special respect to pineal gland innervation. Histochemistry 85:321–325

    Google Scholar 

  • Schröder H, Vollrath L (1986) Neuropeptide Y (NPY)-like immunoreactivity in the guinea pig pineal organ. Neurosci Lett 63:285–289

    Google Scholar 

  • Sheikh SP, Roach E, Fuhlendorf J, Williams J (1991) Localization of y1 receptors for NPY and PYY on vascular smooth muscle cells in rat pancreas. Am J Physiol (in press)

  • Shiotani Y, Yamano M, Shiosaka S, Emson PC, Hillyard CJ, Girgis S, MacIntyre I (1986) Distribution and origins of substance P(SP)-, calcitonin gene-related peptide (CGRP)-, vasoactive intestinal polypeptide (VIP)- and neuropeptide Y (NPY)-containing nerve fibers in the pineal gland of gerbils. Neurosci Lett 70:187–192

    Google Scholar 

  • Sundler F, Moghimzadeh E, Håkanson R, Eklund M, Emson R (1983) Nerve fibers in the gut and pancreas of the rat displaying neuropeptide Y immunoreactivity. Intrinsic and extrinsic origin. Cell Tissue Res 230:487–493

    Google Scholar 

  • Suzuki N, Hardebo JE, Kåhrstrom J, Owman C (1990) Neuropeptide Y co-exists with vasoactive intestinal polypeptide in parasympathetic cerebrovascular nerves originating in the sphenopalatine, otic, and internal carotid ganglia of the rat. Neurosci 36:507–519

    Google Scholar 

  • Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y — a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659–660

    Google Scholar 

  • Udenfriend S, Cooper JR, Clark CT, Baer JE (1953) Rate of turnover of epinephrine in the adrenal medulla. Science 117:663–665

    Google Scholar 

  • Vacas MI, Sarmiento MIK, Pereyra EN, Etchegoyen GS, Cardinali DP (1987) In vitro effects of neuropeptide Y on melatonin and norepinephrine release in rat pineal gland. Cell Mol Neurobiol 7:309–315

    Google Scholar 

  • Wahlestedt C, Yanaihara N, Håkanson R (1986) Evidence for different pre- and postjunctional receptors for neuropeptide Y and related peptides. Regul Pept 13:307–318

    Google Scholar 

Download references

Author information

Author notes

  1. En-Tan Zhang

    Present address: Department of Anatomy, Beijing Medical University, 100083, Beijing, People's Republic of China

Authors and Affiliations

  1. Institute of Medical Anatomy, Department B, The Panum Institute, University of Copenhagen, Blegdamsvej 3, DK-2200, Copenhagen N, Denmark

    En-Tan Zhang, Jens D. Mikkelsen & Morten Møller

Authors
  1. En-Tan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jens D. Mikkelsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Morten Møller
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, ET., Mikkelsen, J.D. & Møller, M. Tyrosine hydroxylase- and neuropeptide Y-immunoreactive nerve fibers in the pineal complex of untreated rats and rats following removal of the superior cervical ganglia. Cell Tissue Res 265, 63–71 (1991). https://doi.org/10.1007/BF00318140

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318140

Key words

Search

Navigation