Experiments on sagittal hippocampus slices from male Wistar rats addressed the effects of 10 nM neuropeptide Y on the level of electrical activity in neurons in the suprachiasmatic nucleus and parameters of spike-based information encoding. Application of neuropeptide Y led to a decrease in the action potential generation frequency in 35 of the 81 neurons recorded; eight cells showed increases in this parameter, and the remaining 38 neurons showed no change in the level of spike activity. The decrease in the spike generation frequency in suprachiasmatic nucleus neurons was accompanied by increases in the entropy of the distribution of interspike intervals and the mutual information between adjacent interspike intervals, which is evidence for increases in the degree of irregularity in these intervals and the patterning of spike information in response to neuropeptide Y. These results demonstrate the ability of neuropeptide Y to modulate the activity level and affect the spike code in the relatively numerous population of neurons in the circadian oscillator of the suprachiasmatic nucleus.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
E. B. Arushanyan and A. V. Popov, “Current concepts of the role of the suprachiasmatic nucleus of the hypothalamus in in the organization of the daily periodism of physiological functions,” Usp. Fiziol. Nauk., 42, No. 4, 39–58 (2011).
C. Acuna-Goycolea, N. Tamamaki, Y. Yanagawa, et al., “Mechanisms of neuropeptide Y, peptide YY, pancreatic polypeptide inhibition of identifi ed green fl uorescent protein-expressing GABA neurons in the hypothalamic neuroendocrine arcuate nucleus,” J. Neurosci., 25, 7406–7419 (2005).
R. C. Besing, L. M. Hablitz, J. R. Paul, et al., “NPY-induced phase shifts of PER2: Luc rhythms are mediated by long-term suppression of neuronal excitability in a phase-specific manner,” Chronobiol. Int., 29, 91–102 (2012).
G. S. Bhumbra and R. E. Dyball, “Measuring spike coding in the rat supraoptic nucleus,” J. Physiol., 555, 281–296 (2003).
G. S. Bhumbra and R. E. D. Dyball, “Assessment of spike activity in the supraoptic nucleus,” J. Neuroendocrinol., 16, 390–397 (2004).
G. S. Bhumbra, A. N. Inyushkin, K. Saeb-Parsy, et al., “Rhythmic changes in spike coding in the rat suprachiasmatic nucleus,” J. Physiol., 653, 291–307 (2005).
T. M. Brown, A. N. Coogan, D. J. Dutler, et al., “Electrophysiological actions of orexins on rat suprachiasmatic neurons in vitro,” Neurosci. Lett., 448, 273–278 (2008).
K. Edelstain and S. Amir, “The role of the intergeniculate leafl et in entrainment of circadian rhythms to a skeleton photoperiod,” J. Neurosci., 19, 372–380 (1999).
D. A. Golombek and R. E. Rosenstein, “Physiology of circadian entrainment,” Physiol. Rev., 90, 1063–1102 (2010).
V. K. Gribkoff, R. L. Pieschl, T. A. Wisialowski, et al., “Phase shifting of circadian rhythms and depression of neuronal activity in the rat suprachiasmatic nucleus by neuropeptide Y mediation by different receptor subtypes,” J. Neurosci., 18, 3014–3022 (1998).
A. C. Hall, G. Earle-Cruikshanks, and M. E. Harrington, “Role of membrane conductances and protein synthesis in subjective day phase advances of the hamster circadian dock by neuropeptide Y,” Eur. J. Neurosci., 11, 3424–3432 (1999).
M. E. Harrington and S. Hoque, “NPY opposes PACAP phase shifts via receptors different from those involved in NPY phase shifts,” NeuroReport, 8, 2677–2680 (1997).
A. N. Inyushkin, G. S. Bhumbra, and R. E. D. Dyball, “Leptin modulates spike coding in the rat suprachiasmatic nucleus,” J. Neuroendocrinol., 21, 705–714 (2009).
A. N. Inyushkin, G. S. Bhumbra, J. A. Gonzalez, and R. E. D. Dyball, “Melatonin modulates spike coding in the rat suprachiasmatic nucleus,” J. Neuroendocrinol., 19, 671–681 (2007).
M. H Hastings, M. Brancaccio, and E. S. Maywood, “Circadian pacemaking in cells and circuits of the suprachiasmatic nucleus,” J. Neuroendocrinol., 26, 2–10 (2014).
A. C. Jackson, G. L. Yao, and B. P. Bean, “Mechanism of spontaneous firing in dorsomedial suprachiasmatic nucleus neurons,” J. Neurosci., 24, 7985–7998 (2004).
D. Janik and N. Mrosovsky, “Intergeniculate leafl et lesions and behaviorally-induced shifts of circadian rhythms,” Brain Res., 651, 174–182 (1994).
R. F. Johnson, L. Smale, R. Y. Moore, and L. P. Morin, “Lateral geniculate lesions block circadian phase-shift responses to a benzodiazepine,” Proc. Natl. Acad. Sci. USA, 85, 5301–5304 (1988).
N. I. Kononenko and F. E. Dudek, “Mechanism of irregular firing of suprachiasmatic nucleus neurons in rat hypothalamic slices,” J. Neurophysiol., 91, 267–273 (2004).
L. K. Laemle, N. Hori, N. L. Strominger, et al., “Physiological and anatomical properties of the suprachiasmatic nucleus of an anophtalmic mouse,” Brain Res., 953, 73–81 (2002).
P. J. Larsen and P. Kristensen, “Distribution of neuropeptide Y receptor expression in the rat suprachiasmatic nucleus,” Mol. Brain Res., 60, 69–76 (1998).
S. Y. Liou and H. E. Albers, “Single unit response of neurons within the hamster suprachiasmatic nucleus to neuropeptide Y,” Brain Res. Bull., 27, 825–828 (1991).
L. P. Morin, “Neuroanatomy of the extended circadian rhythm system,” Exp. Neurol., 243, 4–20 (2013).
L. P. Morin, “The intergeniculate leafl et, but not the visual midbrain, mediates hamster circadian rhythm response to constant light,” J. Biol. Rhythms, 17, 217–226 (2002).
M. F. Paredes, J. Greenwood, and S. C. Baraban, “Neuropeptide Y modulates a G protein-coupled inwardly rectifying potassium current in the mouse hippocampus,” Neurosci. Lett., 340, 9–12 (2003).
C. M. A. Pennartz, M. T. G. De Jeu, A. M. S. Geurtsen, et al., “Electrophysiological and morphological heterogeneity of neurons in slices of rat suprachiasmatic nucleus,” J. Physiol., 506, 775–793 (1998).
B. Rusak, J. H. Meijer, and M. E. Harrington, “Hamster circadian rhythms are phase-shifted by electrical stimulation of the geniculo-hypothalamic tract,” Brain Res., 493, 283–291 (1989).
N. Saderi, F. Cazarez-Marquez, F. N. Buijs, et al., “The NPY intergeniculate leafl et projections to the suprachiasmatic nucleus transmit metabolic conditions,” Neuroscience, 246, 291–300 (2013).
K. M. Schak, S. P. Scordilis, G. Ferreyra, and M. E. Harrington, “Neuropeptide Y activates protein kinase C in hamster suprachiasmatic nuclei brain slices,” Biol. Rhythm Res., 32, 201–206 (2001).
C. Shannon and W. Weaver, The Mathematical Theory of Communication, University of Illinois Press, Urbana (1949).
L. Sosulina, G. Schwesig, G. Seifert, and H. C. Pape, “Neuropeptide Y activates a G-protein-coupled inwardly rectifying potassium current and dampens excitability in the lateral amygdala,” Mol. Cell. Neurosci., 39, 491–498 (2008).
A. M. Thomson and D. C. West, “Factors affecting slow regular firing in the suprachiasmatic nucleus in vitro,” J. Biol. Rhythms, 5, 59–75 (1990).
A. N. van der Pol, K. Obrietan, G. Chen, and A. B. Belousov, “Neuropeptide Y-mediated long-term depression of excitatory activity in suprachiasmatic nucleus neurons,” J. Neurosci., 16, 5883–5895 (1996).
D. H. Weinberg, D. J. Sirinathsinghji, C. P. Tan, et al., “Cloning and expression of a novel neuropeptide Y receptor,” J. Biol. Chem., 271, 16435–16438 (1996).
C. R. Wickland and F. W. Turek, “Lesions of the intergeniculate leaflet block activity-induced phase shifts in the circadian rhythm of activity in the golden hamster,” Brain Res., 660, 283–300 (1994).
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 101, No. 11, pp. 1257–1269, November, 2015.
Rights and permissions
About this article
Cite this article
Inyushkin, A.N., Petrova, A.A., Tkacheva, M.A. et al. Effects of Neuropeptide Y on Neuron Spike Activity in the Rat Suprachiasmatic Nucleus in Vitro. Neurosci Behav Physi 47, 337–344 (2017). https://doi.org/10.1007/s11055-017-0402-6
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11055-017-0402-6