Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate.

The mammalian biological clock, located in the hypothalamic suprachiasmatic nuclei (SCN), imposes its temporal structure on the organism via neural and endocrine outputs. To further investigate SCN control of the autonomic nervous system we focused in the present study on the daily rhythm in plasma...

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Autores principales: Andries Kalsbeek, Ewout Foppen, Ingrid Schalij, Caroline Van Heijningen, Jan van der Vliet, Eric Fliers, Ruud M Buijs
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Publicado: Public Library of Science (PLoS) 2008
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spelling oai:doaj.org-article:5de97b57f5314f0ab1537a5aa553b8fd2021-11-25T06:18:37ZCircadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate.1932-620310.1371/journal.pone.0003194https://doaj.org/article/5de97b57f5314f0ab1537a5aa553b8fd2008-09-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18791643/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203The mammalian biological clock, located in the hypothalamic suprachiasmatic nuclei (SCN), imposes its temporal structure on the organism via neural and endocrine outputs. To further investigate SCN control of the autonomic nervous system we focused in the present study on the daily rhythm in plasma glucose concentrations. The hypothalamic paraventricular nucleus (PVN) is an important target area of biological clock output and harbors the pre-autonomic neurons that control peripheral sympathetic and parasympathetic activity. Using local administration of GABA and glutamate receptor (ant)agonists in the PVN at different times of the light/dark-cycle we investigated whether daily changes in the activity of autonomic nervous system contribute to the control of plasma glucose and plasma insulin concentrations. Activation of neuronal activity in the PVN of non-feeding animals, either by administering a glutamatergic agonist or a GABAergic antagonist, induced hyperglycemia. The effect of the GABA-antagonist was time dependent, causing increased plasma glucose concentrations only when administered during the light period. The absence of a hyperglycemic effect of the GABA-antagonist in SCN-ablated animals provided further evidence for a daily change in GABAergic input from the SCN to the PVN. On the other hand, feeding-induced plasma glucose and insulin responses were suppressed by inhibition of PVN neuronal activity only during the dark period. These results indicate that the pre-autonomic neurons in the PVN are controlled by an interplay of inhibitory and excitatory inputs. Liver-dedicated sympathetic pre-autonomic neurons (responsible for hepatic glucose production) and pancreas-dedicated pre-autonomic parasympathetic neurons (responsible for insulin release) are controlled by inhibitory GABAergic contacts that are mainly active during the light period. Both sympathetic and parasympathetic pre-autonomic PVN neurons also receive excitatory inputs, either from the biological clock (sympathetic pre-autonomic neurons) or from non-clock areas (para-sympathetic pre-autonomic neurons), but the timing information is mainly provided by the GABAergic outputs of the biological clock.Andries KalsbeekEwout FoppenIngrid SchalijCaroline Van HeijningenJan van der VlietEric FliersRuud M BuijsPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 3, Iss 9, p e3194 (2008)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Andries Kalsbeek
Ewout Foppen
Ingrid Schalij
Caroline Van Heijningen
Jan van der Vliet
Eric Fliers
Ruud M Buijs
Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate.
description The mammalian biological clock, located in the hypothalamic suprachiasmatic nuclei (SCN), imposes its temporal structure on the organism via neural and endocrine outputs. To further investigate SCN control of the autonomic nervous system we focused in the present study on the daily rhythm in plasma glucose concentrations. The hypothalamic paraventricular nucleus (PVN) is an important target area of biological clock output and harbors the pre-autonomic neurons that control peripheral sympathetic and parasympathetic activity. Using local administration of GABA and glutamate receptor (ant)agonists in the PVN at different times of the light/dark-cycle we investigated whether daily changes in the activity of autonomic nervous system contribute to the control of plasma glucose and plasma insulin concentrations. Activation of neuronal activity in the PVN of non-feeding animals, either by administering a glutamatergic agonist or a GABAergic antagonist, induced hyperglycemia. The effect of the GABA-antagonist was time dependent, causing increased plasma glucose concentrations only when administered during the light period. The absence of a hyperglycemic effect of the GABA-antagonist in SCN-ablated animals provided further evidence for a daily change in GABAergic input from the SCN to the PVN. On the other hand, feeding-induced plasma glucose and insulin responses were suppressed by inhibition of PVN neuronal activity only during the dark period. These results indicate that the pre-autonomic neurons in the PVN are controlled by an interplay of inhibitory and excitatory inputs. Liver-dedicated sympathetic pre-autonomic neurons (responsible for hepatic glucose production) and pancreas-dedicated pre-autonomic parasympathetic neurons (responsible for insulin release) are controlled by inhibitory GABAergic contacts that are mainly active during the light period. Both sympathetic and parasympathetic pre-autonomic PVN neurons also receive excitatory inputs, either from the biological clock (sympathetic pre-autonomic neurons) or from non-clock areas (para-sympathetic pre-autonomic neurons), but the timing information is mainly provided by the GABAergic outputs of the biological clock.
format article
author Andries Kalsbeek
Ewout Foppen
Ingrid Schalij
Caroline Van Heijningen
Jan van der Vliet
Eric Fliers
Ruud M Buijs
author_facet Andries Kalsbeek
Ewout Foppen
Ingrid Schalij
Caroline Van Heijningen
Jan van der Vliet
Eric Fliers
Ruud M Buijs
author_sort Andries Kalsbeek
title Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate.
title_short Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate.
title_full Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate.
title_fullStr Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate.
title_full_unstemmed Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate.
title_sort circadian control of the daily plasma glucose rhythm: an interplay of gaba and glutamate.
publisher Public Library of Science (PLoS)
publishDate 2008
url https://doaj.org/article/5de97b57f5314f0ab1537a5aa553b8fd
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