Altered entrainment to the day/night cycle attenuates the daily rise in circulating corticosterone in the mouse

Patricia J. Sollars, Michael J. Weiser, Andrea E. Kudwa, Jayne R. Bramley, Malcolm D. Ogilvie, Robert L. Spencer, Robert J Handa, Gary E. Pickard

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

The suprachiasmatic nucleus (SCN) is a circadian oscillator entrained to the day/night cycle via input from the retina. Serotonin (5-HT) afferents to the SCN modulate retinal signals via activation of 5-HT1B receptors, decreasing responsiveness to light. Consequently, 5-HT1B receptor knockout (KO) mice entrain to the day/night cycle with delayed activity onsets. Since circulating corticosterone levels exhibit a robust daily rhythm peaking around activity onset, we asked whether delayed entrainment of activity onsets affects rhythmic corticosterone secretion. Wheel-running activity and plasma corticosterone were monitored in mice housed under several different lighting regimens. Both duration of the light:dark cycle (T cycle) and the duration of light within that cycle was altered. 5-HT1B KO mice that entrained to a 9.5L:13.5D (short day in a T = 23 h) cycle with activity onsets delayed more than 4 h after light offset exhibited a corticosterone rhythm in phase with activity rhythms but reduced 50% in amplitude compared to animals that initiated daily activity <4 h after light offset. Wild type mice in 8L:14D (short day in a T = 22 h) conditions with highly delayed activity onsets also exhibited a 50% reduction in peak plasma corticosterone levels. Exogenous adrenocorticotropin (ACTH) stimulation in animals exhibiting highly delayed entrainment suggested that the endogenous rhythm of adrenal responsiveness to ACTH remained aligned with SCN-driven behavioral activity. Circadian clock gene expression in the adrenal cortex of these same animals suggested that the adrenal circadian clock was also aligned with SCN-driven behavior. Under T cycles <24 h, altered circadian entrainment to short day (winter-like) conditions, manifest as long delays in activity onset after light offset, severely reduces the amplitude of the diurnal rhythm of plasma corticosterone. Such a pronounced reduction in the glucocorticoid rhythm may alter rhythmic gene expression in the central nervous system and in peripheral organs contributing to an array of potential pathophysiologies.

Original languageEnglish (US)
Article numbere111944
JournalPLoS One
Volume9
Issue number11
DOIs
StatePublished - Nov 3 2014

Fingerprint

corticosterone
Corticosterone
Suprachiasmatic Nucleus
mice
corticotropin
Adrenocorticotropic Hormone
circadian rhythm
Receptor, Serotonin, 5-HT1B
Light
Circadian Clocks
Animals
Photoperiod
Plasmas
serotonin
Gene expression
Knockout Mice
Clocks
Serotonin
Activity Cycles
Gene Expression

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Sollars, P. J., Weiser, M. J., Kudwa, A. E., Bramley, J. R., Ogilvie, M. D., Spencer, R. L., ... Pickard, G. E. (2014). Altered entrainment to the day/night cycle attenuates the daily rise in circulating corticosterone in the mouse. PLoS One, 9(11), [e111944]. https://doi.org/10.1371/journal.pone.0111944

Altered entrainment to the day/night cycle attenuates the daily rise in circulating corticosterone in the mouse. / Sollars, Patricia J.; Weiser, Michael J.; Kudwa, Andrea E.; Bramley, Jayne R.; Ogilvie, Malcolm D.; Spencer, Robert L.; Handa, Robert J; Pickard, Gary E.

In: PLoS One, Vol. 9, No. 11, e111944, 03.11.2014.

Research output: Contribution to journalArticle

Sollars, PJ, Weiser, MJ, Kudwa, AE, Bramley, JR, Ogilvie, MD, Spencer, RL, Handa, RJ & Pickard, GE 2014, 'Altered entrainment to the day/night cycle attenuates the daily rise in circulating corticosterone in the mouse', PLoS One, vol. 9, no. 11, e111944. https://doi.org/10.1371/journal.pone.0111944
Sollars, Patricia J. ; Weiser, Michael J. ; Kudwa, Andrea E. ; Bramley, Jayne R. ; Ogilvie, Malcolm D. ; Spencer, Robert L. ; Handa, Robert J ; Pickard, Gary E. / Altered entrainment to the day/night cycle attenuates the daily rise in circulating corticosterone in the mouse. In: PLoS One. 2014 ; Vol. 9, No. 11.
@article{175335768dc946c1a5ecf314d2de5e89,
title = "Altered entrainment to the day/night cycle attenuates the daily rise in circulating corticosterone in the mouse",
abstract = "The suprachiasmatic nucleus (SCN) is a circadian oscillator entrained to the day/night cycle via input from the retina. Serotonin (5-HT) afferents to the SCN modulate retinal signals via activation of 5-HT1B receptors, decreasing responsiveness to light. Consequently, 5-HT1B receptor knockout (KO) mice entrain to the day/night cycle with delayed activity onsets. Since circulating corticosterone levels exhibit a robust daily rhythm peaking around activity onset, we asked whether delayed entrainment of activity onsets affects rhythmic corticosterone secretion. Wheel-running activity and plasma corticosterone were monitored in mice housed under several different lighting regimens. Both duration of the light:dark cycle (T cycle) and the duration of light within that cycle was altered. 5-HT1B KO mice that entrained to a 9.5L:13.5D (short day in a T = 23 h) cycle with activity onsets delayed more than 4 h after light offset exhibited a corticosterone rhythm in phase with activity rhythms but reduced 50{\%} in amplitude compared to animals that initiated daily activity <4 h after light offset. Wild type mice in 8L:14D (short day in a T = 22 h) conditions with highly delayed activity onsets also exhibited a 50{\%} reduction in peak plasma corticosterone levels. Exogenous adrenocorticotropin (ACTH) stimulation in animals exhibiting highly delayed entrainment suggested that the endogenous rhythm of adrenal responsiveness to ACTH remained aligned with SCN-driven behavioral activity. Circadian clock gene expression in the adrenal cortex of these same animals suggested that the adrenal circadian clock was also aligned with SCN-driven behavior. Under T cycles <24 h, altered circadian entrainment to short day (winter-like) conditions, manifest as long delays in activity onset after light offset, severely reduces the amplitude of the diurnal rhythm of plasma corticosterone. Such a pronounced reduction in the glucocorticoid rhythm may alter rhythmic gene expression in the central nervous system and in peripheral organs contributing to an array of potential pathophysiologies.",
author = "Sollars, {Patricia J.} and Weiser, {Michael J.} and Kudwa, {Andrea E.} and Bramley, {Jayne R.} and Ogilvie, {Malcolm D.} and Spencer, {Robert L.} and Handa, {Robert J} and Pickard, {Gary E.}",
year = "2014",
month = "11",
day = "3",
doi = "10.1371/journal.pone.0111944",
language = "English (US)",
volume = "9",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "11",

}

TY - JOUR

T1 - Altered entrainment to the day/night cycle attenuates the daily rise in circulating corticosterone in the mouse

AU - Sollars, Patricia J.

AU - Weiser, Michael J.

AU - Kudwa, Andrea E.

AU - Bramley, Jayne R.

AU - Ogilvie, Malcolm D.

AU - Spencer, Robert L.

AU - Handa, Robert J

AU - Pickard, Gary E.

PY - 2014/11/3

Y1 - 2014/11/3

N2 - The suprachiasmatic nucleus (SCN) is a circadian oscillator entrained to the day/night cycle via input from the retina. Serotonin (5-HT) afferents to the SCN modulate retinal signals via activation of 5-HT1B receptors, decreasing responsiveness to light. Consequently, 5-HT1B receptor knockout (KO) mice entrain to the day/night cycle with delayed activity onsets. Since circulating corticosterone levels exhibit a robust daily rhythm peaking around activity onset, we asked whether delayed entrainment of activity onsets affects rhythmic corticosterone secretion. Wheel-running activity and plasma corticosterone were monitored in mice housed under several different lighting regimens. Both duration of the light:dark cycle (T cycle) and the duration of light within that cycle was altered. 5-HT1B KO mice that entrained to a 9.5L:13.5D (short day in a T = 23 h) cycle with activity onsets delayed more than 4 h after light offset exhibited a corticosterone rhythm in phase with activity rhythms but reduced 50% in amplitude compared to animals that initiated daily activity <4 h after light offset. Wild type mice in 8L:14D (short day in a T = 22 h) conditions with highly delayed activity onsets also exhibited a 50% reduction in peak plasma corticosterone levels. Exogenous adrenocorticotropin (ACTH) stimulation in animals exhibiting highly delayed entrainment suggested that the endogenous rhythm of adrenal responsiveness to ACTH remained aligned with SCN-driven behavioral activity. Circadian clock gene expression in the adrenal cortex of these same animals suggested that the adrenal circadian clock was also aligned with SCN-driven behavior. Under T cycles <24 h, altered circadian entrainment to short day (winter-like) conditions, manifest as long delays in activity onset after light offset, severely reduces the amplitude of the diurnal rhythm of plasma corticosterone. Such a pronounced reduction in the glucocorticoid rhythm may alter rhythmic gene expression in the central nervous system and in peripheral organs contributing to an array of potential pathophysiologies.

AB - The suprachiasmatic nucleus (SCN) is a circadian oscillator entrained to the day/night cycle via input from the retina. Serotonin (5-HT) afferents to the SCN modulate retinal signals via activation of 5-HT1B receptors, decreasing responsiveness to light. Consequently, 5-HT1B receptor knockout (KO) mice entrain to the day/night cycle with delayed activity onsets. Since circulating corticosterone levels exhibit a robust daily rhythm peaking around activity onset, we asked whether delayed entrainment of activity onsets affects rhythmic corticosterone secretion. Wheel-running activity and plasma corticosterone were monitored in mice housed under several different lighting regimens. Both duration of the light:dark cycle (T cycle) and the duration of light within that cycle was altered. 5-HT1B KO mice that entrained to a 9.5L:13.5D (short day in a T = 23 h) cycle with activity onsets delayed more than 4 h after light offset exhibited a corticosterone rhythm in phase with activity rhythms but reduced 50% in amplitude compared to animals that initiated daily activity <4 h after light offset. Wild type mice in 8L:14D (short day in a T = 22 h) conditions with highly delayed activity onsets also exhibited a 50% reduction in peak plasma corticosterone levels. Exogenous adrenocorticotropin (ACTH) stimulation in animals exhibiting highly delayed entrainment suggested that the endogenous rhythm of adrenal responsiveness to ACTH remained aligned with SCN-driven behavioral activity. Circadian clock gene expression in the adrenal cortex of these same animals suggested that the adrenal circadian clock was also aligned with SCN-driven behavior. Under T cycles <24 h, altered circadian entrainment to short day (winter-like) conditions, manifest as long delays in activity onset after light offset, severely reduces the amplitude of the diurnal rhythm of plasma corticosterone. Such a pronounced reduction in the glucocorticoid rhythm may alter rhythmic gene expression in the central nervous system and in peripheral organs contributing to an array of potential pathophysiologies.

UR - http://www.scopus.com/inward/record.url?scp=84909606599&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84909606599&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0111944

DO - 10.1371/journal.pone.0111944

M3 - Article

C2 - 25365210

AN - SCOPUS:84909606599

VL - 9

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 11

M1 - e111944

ER -