Elsevier

Brain Research

Volume 620, Issue 2, 27 August 1993, Pages 281-286
Brain Research

Suprachiasmatic circadian pacemaker of rat shows two windows of sensitivity to neuropeptide Y in vitro

https://doi.org/10.1016/0006-8993(93)90166-KGet rights and content

Abstract

The geniculohypothalamic tract carries visual information from the intergeniculate leaflet to the suprachiasmatic circadian pacemaker. NPY, found in this projection, has been shown to affect the phase of behavioral rhythms and influence photic entrainment. We now demonstrate that NPY, when briefly applied to the geniculate projection sites of rat SCN in vitro, induces permanent phase-shifts in the rhythm of neuronal electrical activity at two separate phases of the circadian cycle.

References (67)

  • JohnsonR.F. et al.

    Lateral geniculate lesions alter circadian activity rhythms in the hamster

    Brain Res. Bull.

    (1989)
  • MasonR. et al.

    Electrophysiological responses of hamster suprachiasmatic neurones to neuropeptide Y in the hypothalamic slice preparation

    Neurosci. Lett.

    (1987)
  • McArthurA.J. et al.

    Melatonin directly resets the suprachiasmatic circadian clock in vitro

    Brain Res.

    (1991)
  • MikkelsenJ.D. et al.

    A direct neural projection from the intergeniculate leaflet of the lateral geniculate to the deep pineal gland of the rat, demonstrated withPhaseolus vulgaris leucagglutinin

    Brain Res.

    (1990)
  • MikkelsenJ.D. et al.

    An immunohistochemical and chromatographic analysis of the distribution and processing of neuropeptide Y in the rat suprachiasmatic nucleus

    Peptides

    (1991)
  • MillhouseO.E.

    Optic chiasm collaterals afferent to the suprachiasmatic nucleus

    Brain Res.

    (1977)
  • MooreR.Y. et al.

    GABA is the principle neurotransmitter in the circadian timing system

    Neurosci. Lett.

    (1993)
  • PickardG.E.

    Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suprachiasmatic nucleus and the intergeniculate leaflet of the thalamus

    Neurosci. Lett.

    (1985)
  • PickardG.E.

    Entrainment of the circadian rhythm of wheel-running activity is phase-shifted by ablation of the intergeniculate leaflet

    Brain Res.

    (1989)
  • ProsserR.A. et al.

    A serotonin agonist phase-shifts the circadian clock in the suprachiasmatic nuclei in vitro

    Brain Res.

    (1990)
  • ShibataS. et al.

    Influence of environmental light-dark cycle and enucleation on activity of suprachiasmatic neurons in slice preparation

    Brain Res.

    (1984)
  • StanleyB.G. et al.

    Neuropeptide Y: stimulation of feeding and drinking by injection into the paraventricular nucleus

    Life Sci.

    (1984)
  • TakatsujiK. et al.

    The organization of the rat lateral geniculate body by immunohistochemical analysis of neuroactive substances

    Brain Res.

    (1989)
  • AlbersH.E.

    Response of hamster circadian system to transitions between light and darkness

    Am. J. Physiol.

    (1986)
  • AlbersH.E. et al.

    Neuropeptide Y in the hypothalamus: effects on corticosterone and single-unit activity

    Am. J. Physiol.

    (1990)
  • AllenY.S. et al.

    Neuropeptide Y distribution in the rat brain

    Science

    (1983)
  • BoulosZ. et al.

    Circadian phase-response curves for dark pulses in the hamster

    J. Comp. Physiol.

    (1982)
  • CardJ.P. et al.

    Ventral lateral geniculate nucleus efferents to the rat suprachiasmatic nucleus exhibit avian pancreatic polypeptide-like immunoreactivity

    J. Comp. Neurol.

    (1982)
  • CardJ.P. et al.

    Organization of the lateral geniculate-hypothalamic connections in the rat

    J. Comp. Neurol.

    (1989)
  • ClarkJ.T. et al.

    Neuropeptide Y and human pancreatic polypeptide stimulate feeding behaviors in the rat

    Endocrinology

    (1984)
  • CropperE.C. et al.

    An immunocytochemical study of the serotonergic innervation of the thalamus of the rat

    J. Comp. Neurol.

    (1984)
  • De QuidtM.E. et al.

    Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system-II

    Neuroscience

    (1986)
  • GilletteM.U.

    SCN electrophysiology in vitro

  • Cited by (55)

    • Neuropeptide Y Y2 antagonist treated ovariectomized mice exhibit greater bone mineral density

      2018, Neuropeptides
      Citation Excerpt :

      NPY is processed from a 94–95-amino acid prohormone and has been classified into the same family as peptide YY and pancreatic polypeptide (Balasubramaniam, 1997; Tatemoto et al., 1982). Since its original isolation, it has been linked to numerous processes such as inhibiting anxiety and depression (Heilig, 2004), regulating learning-associated synaptic plasticity (Redrobe et al., 2004; Thorsell et al., 2000), and modulating circadian rhythm (Medanic and Gillette, 1993; Yannielli and Harrington, 2001), vascular smooth muscle contraction (Glenn and Duckles, 1994; Pernow and Lundberg, 1988) and pain transmission (Naveilhan et al., 2001; Solway et al., 2011). In humans, NPY mediates its effects by interacting with a diverse family of G-protein coupled receptors (Y1, Y2, Y4, Y5), which are highly expressed across a number of different brain regions and throughout the sympathetic nervous system (Blomqvist and Herzog, 1997; Brothers and Wahlestedt, 2010; Fetissov et al., 2004b; Jacques et al., 1997; Nozdrachev and Masliukov, 2011; Redrobe et al., 2002).

    • Timing, sleep, and respiration in health and disease

      2013, Progress in Molecular Biology and Translational Science
      Citation Excerpt :

      Just as the reason that these stimuli are able to shift the clock is not clear, the mechanisms are also not clear. The neurotransmitters serotonin (5-HT), neuropeptide Y,134 pituitary adenylate cyclase activating polypeptide,135,136 and substance P have all been shown to affect the timing of the circadian clock when presented during the middle of the subjective daytime. Serotonin can advance the timing of the peak in single-unit neuronal firing in rat hypothalamic slices in vitro137 and in the timing of the onset of hamster wheel-running activity when applied into the cerebral ventricles or directly to the SCN in vivo.138

    • Biological timekeeping

      2012, Sleep Medicine Clinics
      Citation Excerpt :

      The GHT contains neuropeptide Y (NPY) and GABA. NPY is believed to be involved in activity-induced phase shifts during the daytime in nocturnal animals but also seems to be able to modulate light-induced phase shifts.32–34 However, although the GHT pathway can transmit photic signals, disruption of this pathway does not prevent entrainment.35

    • Feedback actions of locomotor activity to the circadian clock

      2012, Progress in Brain Research
      Citation Excerpt :

      Infusion of NPY into the region of the SCN in vivo and directly onto SCN slices in vitro suppresses per1 and per2 expression (Fukuhara et al., 2001; Maywood et al., 2002); an effect mediated by NPY Y1/Y5 and Y2 receptors. NPY application to cultured SCN slices in vitro also induces nonphotic-like phase shifts in electrical activity as well as acute suppression of SCN firing (Cutler et al., 1998; Gribkoff et al., 1998; Medanic and Gillette, 1993; Shibata and Moore, 1993; van den Pol et al., 1996). The GABAergic nature of IGL neurons, including those that give rise to the GHT, further supports a role for the IGL/GHT in nonphotic signaling, given, as mentioned earlier, that the GABAA agonist muscimol also produces nonphotic phase-shifting responses when infused centrally to hamsters (Smith et al., 1989).

    View all citing articles on Scopus

    Support of AFOSR Grant 90-0205 to M.U.G. and NIH Grant T32 GMO7143 to M.M. is gratefully acknowledged.

    *

    We would like to thank Dr. Eve Gallman and Angela J. McArthur for their helpful discussions.

    View full text