The Role of Adenosine in the Maturation of Sleep Homeostasis in Rats

Overview

Journal J Neurophysiol

Publisher American Physiological Society

Specialties Neurology
Physiology

Date 2016 Oct 28

PMID 27784808

Citations 10

Authors

Irma Gvilia

Natalia Suntsova

Andrey Kostin

Anna Kalinchuk

Dennis McGinty

Radhika Basheer

Ronald Szymusiak

Affiliations

Soon will be listed here.

Abstract

New & Noteworthy: Brain mechanisms that regulate the maturation of sleep are understudied. The present study generated first evidence about a potential mechanistic role for adenosine in the maturation of sleep homeostasis. Specifically, we demonstrate that early postweaning development in rats, when homeostatic response to sleep loss become adult like, is characterized by maturational changes in wake-related production/release of adenosine in the brain. Pharmacologically increased adenosine signaling in developing brain facilitates homeostatic responses to sleep deprivation.

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References

Gong H, McGinty D, Guzman-Marin R, Chew K, Stewart D, Szymusiak R . Activation of c-fos in GABAergic neurones in the preoptic area during sleep and in response to sleep deprivation. J Physiol. 2004; 556(Pt 3):935-46. PMC: 1664995. DOI: 10.1113/jphysiol.2003.056622. View

Seelke A, Blumberg M . The microstructure of active and quiet sleep as cortical delta activity emerges in infant rats. Sleep. 2008; 31(5):691-9. PMC: 2398759. DOI: 10.1093/sleep/31.5.691. View

Sherin J, Shiromani P, McCarley R, Saper C . Activation of ventrolateral preoptic neurons during sleep. Science. 1996; 271(5246):216-9. DOI: 10.1126/science.271.5246.216. View

Szymusiak R, Alam N, Steininger T, McGinty D . Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Res. 1998; 803(1-2):178-88. DOI: 10.1016/s0006-8993(98)00631-3. View

Kalinchuk A, McCarley R, Porkka-Heiskanen T, Basheer R . The time course of adenosine, nitric oxide (NO) and inducible NO synthase changes in the brain with sleep loss and their role in the non-rapid eye movement sleep homeostatic cascade. J Neurochem. 2010; 116(2):260-72. PMC: 3042163. DOI: 10.1111/j.1471-4159.2010.07100.x. View

Kalinchuk A, McCarley R, Stenberg D, Porkka-Heiskanen T, Basheer R . The role of cholinergic basal forebrain neurons in adenosine-mediated homeostatic control of sleep: lessons from 192 IgG-saporin lesions. Neuroscience. 2008; 157(1):238-53. PMC: 3678094. DOI: 10.1016/j.neuroscience.2008.08.040. View

Basheer R, Strecker R, Thakkar M, McCarley R . Adenosine and sleep-wake regulation. Prog Neurobiol. 2004; 73(6):379-96. DOI: 10.1016/j.pneurobio.2004.06.004. View

Yang C, Franciosi S, Brown R . Adenosine inhibits the excitatory synaptic inputs to Basal forebrain cholinergic, GABAergic, and parvalbumin neurons in mice. Front Neurol. 2013; 4:77. PMC: 3687201. DOI: 10.3389/fneur.2013.00077. View

Bjorness T, Dale N, Mettlach G, Sonneborn A, Sahin B, Fienberg A . An Adenosine-Mediated Glial-Neuronal Circuit for Homeostatic Sleep. J Neurosci. 2016; 36(13):3709-21. PMC: 4812131. DOI: 10.1523/JNEUROSCI.3906-15.2016. View

10.

Gramsbergen A . The development of the EEG in the rat. Dev Psychobiol. 1976; 9(6):501-15. DOI: 10.1002/dev.420090604. View

11.

Frank M, Morrissette R, Heller H . Effects of sleep deprivation in neonatal rats. Am J Physiol. 1998; 275(1):R148-57. DOI: 10.1152/ajpregu.1998.275.1.R148. View

12.

Porkka-Heiskanen T, Alanko L, Kalinchuk A, Stenberg D . Adenosine and sleep. Sleep Med Rev. 2003; 6(4):321-32. DOI: 10.1053/smrv.2001.0201. View

13.

Weaver D . A1-adenosine receptor gene expression in fetal rat brain. Brain Res Dev Brain Res. 1996; 94(2):205-23. View

14.

Kalinchuk A, Porkka-Heiskanen T, McCarley R, Basheer R . Cholinergic neurons of the basal forebrain mediate biochemical and electrophysiological mechanisms underlying sleep homeostasis. Eur J Neurosci. 2014; 41(2):182-95. PMC: 4460789. DOI: 10.1111/ejn.12766. View

15.

Savelyev S, Rantamaki T, Rytkonen K, Castren E, Porkka-Heiskanen T . Sleep homeostasis and depression: studies with the rat clomipramine model of depression. Neuroscience. 2012; 212:149-58. DOI: 10.1016/j.neuroscience.2012.03.029. View

16.

Gvilia I, Suntsova N, Angara B, McGinty D, Szymusiak R . Maturation of sleep homeostasis in developing rats: a role for preoptic area neurons. Am J Physiol Regul Integr Comp Physiol. 2011; 300(4):R885-94. PMC: 3075078. DOI: 10.1152/ajpregu.00727.2010. View

17.

Gvilia I, Turner A, McGinty D, Szymusiak R . Preoptic area neurons and the homeostatic regulation of rapid eye movement sleep. J Neurosci. 2006; 26(11):3037-44. PMC: 6673979. DOI: 10.1523/JNEUROSCI.4827-05.2006. View

18.

Arrigoni E, Chamberlin N, Saper C, McCarley R . Adenosine inhibits basal forebrain cholinergic and noncholinergic neurons in vitro. Neuroscience. 2006; 140(2):403-13. DOI: 10.1016/j.neuroscience.2006.02.010. View

19.

Thakkar M, Delgiacco R, Strecker R, McCarley R . Adenosinergic inhibition of basal forebrain wakefulness-active neurons: a simultaneous unit recording and microdialysis study in freely behaving cats. Neuroscience. 2003; 122(4):1107-13. DOI: 10.1016/j.neuroscience.2003.08.006. View

20.

Bjorness T, Kelly C, Gao T, Poffenberger V, Greene R . Control and function of the homeostatic sleep response by adenosine A1 receptors. J Neurosci. 2009; 29(5):1267-76. PMC: 2754857. DOI: 10.1523/JNEUROSCI.2942-08.2009. View