View Item 

Show simple item record

Sleep duration varies as a function of glutamate and GABA in rat pontine reticular formation

dc.contributor.authorWatson, Christopher J.en_US
dc.contributor.authorLydic, Ralphen_US
dc.contributor.authorBaghdoyan, Helen A.en_US
dc.date.accessioned2011-11-10T15:31:15Z
dc.date.available2012-10-01T18:34:16Zen_US
dc.date.issued2011-08en_US
dc.identifier.citationWatson, Christopher J.; Lydic, Ralph; Baghdoyan, Helen A. (2011). "Sleep duration varies as a function of glutamate and GABA in rat pontine reticular formation." Journal of Neurochemistry 118(4). <http://hdl.handle.net/2027.42/86813>en_US
dc.identifier.issn0022-3042en_US
dc.identifier.issn1471-4159en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/86813
dc.description.abstractThe oral part of the pontine reticular formation (PnO) is a component of the ascending reticular activating system and plays a role in the regulation of sleep and wakefulness. The PnO receives glutamatergic and GABAergic projections from many brain regions that regulate behavioral state. Indirect, pharmacological evidence has suggested that glutamatergic and GABAergic signaling within the PnO alters traits that characterize wakefulness and sleep. No previous studies have simultaneously measured endogenous glutamate and GABA from rat PnO in relation to sleep and wakefulness. The present study utilized in vivo microdialysis coupled on‐line to capillary electrophoresis with laser‐induced fluorescence to test the hypothesis that concentrations of glutamate and GABA in the PnO vary across the sleep/wake cycle. Concentrations of glutamate and GABA were significantly higher during wakefulness than during non‐rapid eye movement sleep and rapid eye movement sleep. Regression analysis revealed that decreases in glutamate and GABA accounted for a significant portion of the variance in the duration of non‐rapid eye movement sleep and rapid eye movement sleep episodes. These data provide novel support for the hypothesis that endogenous glutamate and GABA in the PnO contribute to the regulation of sleep duration.en_US
dc.publisherBlackwell Publishing Ltden_US
dc.publisherWiley Periodicals, Inc.en_US
dc.subject.otherCapillary Electrophoresisen_US
dc.subject.otherIn Vivo Microdialysisen_US
dc.subject.otherNREM Sleepen_US
dc.subject.otherREM Sleepen_US
dc.titleSleep duration varies as a function of glutamate and GABA in rat pontine reticular formationen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelNeurosciencesen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Anesthesiology, University of Michigan, Ann Arbor, Michigan, USAen_US
dc.identifier.pmid21679185en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/86813/1/j.1471-4159.2011.07350.x.pdf
dc.identifier.doi10.1111/j.1471-4159.2011.07350.xen_US
dc.identifier.sourceJournal of Neurochemistryen_US
dc.identifier.citedreferenceAlam M. N. and Mallick B. N. ( 1994 ) Role of lateral preoptic area alpha‐1 and alpha‐2 adrenoceptors in sleep‐wakefulness and body temperature regulation. Brain Res. Bull. 35, 171 – 177.en_US
dc.identifier.citedreferenceAngulo M. C., Le Meur K., Kozlov A. S., Charpak S. and Audinat E. ( 2008 ) GABA, a forgotten gliotransmitter. Prog. Neurobiol. 86, 297 – 303.en_US
dc.identifier.citedreferenceAzuma S., Kodama T., Honda K. and Inoue S. ( 1996 ) State‐dependent changes of extracellular glutamate in the medial preoptic area in freely behaving rats. Neurosci. Lett. 214, 179 – 182.en_US
dc.identifier.citedreferenceBaghdoyan H. A., Lydic R., Callaway C. W. and Hobson J. A. ( 1989 ) The carbachol‐induced enhancement of desynchronized sleep signs is dose dependent and antagonized by centrally administered atropine. Neuropsychopharmacology 2, 67 – 79.en_US
dc.identifier.citedreferenceBoissard R., Gervasoni D., Schmidt M. H., Barbagli B., Fort P. and Luppi P. H. ( 2002 ) The rat ponto‐medullary network responsible for paradoxical sleep onset and maintenance: a combined microinjection and functional neuroanatomical study. Eur. J. Neurosci. 16, 1959 – 1973.en_US
dc.identifier.citedreferenceBoissard R., Fort P., Gervasoni D., Barbagli B. and Luppi P. H. ( 2003 ) Localization of the GABAergic and non‐GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. Eur. J. Neurosci. 18, 1627 – 1639.en_US
dc.identifier.citedreferenceBowser M. T. and Kennedy R. T. ( 2001 ) In vivo monitoring of amine neurotransmitters using microdialysis with on‐line capillary electrophoresis. Electrophoresis 22, 3668 – 3676.en_US
dc.identifier.citedreferenceBrevig H. N., Watson C. J., Lydic R. and Baghdoyan H. A. ( 2010 ) Hypocretin and GABA interact in the pontine reticular formation to increase wakefulness. Sleep 33, 1285 – 1293.en_US
dc.identifier.citedreferenceBrown E. N., Lydic R. and Schiff N. D. ( 2010 ) General anesthesia, sleep, and coma. N. Engl. J. Med. 363, 2638 – 2650.en_US
dc.identifier.citedreferenceCamacho‐Arroyo I., Alvarado R., Manjarrez J. and Tapia R. ( 1991 ) Microinjections of muscimol and bicuculline into the pontine reticular formation modify the sleep‐waking cycle in the rat. Neurosci. Lett. 129, 95 – 97.en_US
dc.identifier.citedreferenceCape E. G. and Jones B. E. ( 2000 ) Effects of glutamate agonist versus procaine microinjections into the basal forebrain cholinergic cell area upon gamma and theta EEG activity and sleep‐wake state. Eur. J. Neurosci. 12, 2166 – 2184.en_US
dc.identifier.citedreferenceDash M. B., Douglas C. L., Vyazovskiy V. V., Cirelli C. and Tononi G. ( 2009 ) Long‐term homeostasis of extracellular glutamate in the rat cerebral cortex across sleep and waking states. J. Neurosci. 29, 580 – 589.en_US
dc.identifier.citedreferenceDatta S., Patterson E. H. and Spoley E. E. ( 2001a ) Excitation of the pedunculopontine tegmental NMDA receptors induces wakefulness and cortical activation in the rat. J. Neurosci. Res. 66, 109 – 116.en_US
dc.identifier.citedreferenceDatta S., Spoley E. E. and Patterson E. H. ( 2001b ) Microinjection of glutamate into the pedunculopontine tegmentum induces REM sleep and wakefulness in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R752 – R759.en_US
dc.identifier.citedreferenceDatta S., Spoley E. E., Mavanji V. K. and Patterson E. H. ( 2002 ) A novel role of pedunculopontine tegmental kainate receptors: a mechanism of rapid eye movement sleep generation in the rat. Neuroscience 114, 157 – 164.en_US
dc.identifier.citedreferenceDel Arco A., Segovia G., Fuxe K. and Mora F. ( 2003 ) Changes in dialysate concentrations of glutamate and GABA in the brain: an index of volume transmission mediated actions? J. Neurochem. 85, 23 – 33.en_US
dc.identifier.citedreferenceFendt M., Koch M. and Schnitzler H. U. ( 1996 ) NMDA receptors in the pontine brainstem are necessary for fear potentiation of the startle response. Eur. J. Pharmacol. 318, 1 – 6.en_US
dc.identifier.citedreferenceFerrario C. R., Shou M., Samaha A. N., Watson C. J., Kennedy R. T. and Robinson T. E. ( 2008 ) The rate of intravenous cocaine administration alters c‐fos mRNA expression and the temporal dynamics of dopamine, but not glutamate, overflow in the striatum. Brain Res. 1209, 151 – 156.en_US
dc.identifier.citedreferenceFlint R. R., Chang T., Lydic R. and Baghdoyan H. A. ( 2010 ) GABA(A) receptors in the pontine reticular formation of C57BL/6J mouse modulate neurochemical, electrographic, and behavioral phenotypes of wakefulness. J. Neurosci. 30, 12301 – 12309.en_US
dc.identifier.citedreferenceFung S. J., Xi M., Zhang J., Torterolo P., Sampogna S., Morales F. R. and Chase M. H. ( 2011 ) Projection neurons from the central nucleus of the amygdala to the nucleus pontis oralis. J. Neurosci. Res. 89, 429 – 436.en_US
dc.identifier.citedreferenceGreene R. W. and Carpenter D. O. ( 1985 ) Actions of neurotransmitters on pontine medial reticular formation neurons of cat. J. Neurophysiol. 54, 520 – 531.en_US
dc.identifier.citedreferenceHalassa M. M. and Haydon P. G. ( 2010 ) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 72, 335 – 355.en_US
dc.identifier.citedreferenceHasegawa T., Kohyama J. and Honda K. ( 2003 ) Amino acid release in the rat oral pontine reticular nucleus across various vigilance states. Sleep Biol. Rhythms 1, 195 – 198.en_US
dc.identifier.citedreferenceJohn J., Ramanathan L. and Siegel J. M. ( 2008 ) Rapid changes in glutamate levels in the posterior hypothalamus across sleep‐wake states in freely behaving rats. Am. J. Physiol.-Reg. I 295, R2041 – R2049.en_US
dc.identifier.citedreferenceKaneko T., Itoh K., Shigemoto R. and Mizuno N. ( 1989 ) Glutaminase‐like immunoreactivity in the lower brainstem and cerebellum of the adult rat. Neuroscience 32, 79 – 98.en_US
dc.identifier.citedreferenceKekesi K. A., Dobolyi A., Salfay O., Nyitrai G. and Juhasz G. ( 1997 ) Slow wave sleep is accompanied by release of certain amino acids in the thalamus of cats. Neuroreport 8, 1183 – 1186.en_US
dc.identifier.citedreferenceKodama T. and Honda Y. ( 1999 ) Acetylcholine and glutamate release during sleep‐wakefulness in the pedunculopontine tegmental nucleus and norepinephrine changes regulated by nitric oxide. Psychiatry Clin. Neurosci. 53, 109 – 111.en_US
dc.identifier.citedreferenceKodama T., Lai Y. Y. and Siegel J. M. ( 1998 ) Enhanced glutamate release during REM sleep in the rostromedial medulla as measured by in vivo microdialysis. Brain Res. 780, 178 – 181.en_US
dc.identifier.citedreferenceKrase W., Koch M. and Schnitzler H. U. ( 1993 ) Glutamate antagonists in the reticular formation reduce the acoustic startle response. Neuroreport 4, 13 – 16.en_US
dc.identifier.citedreferenceLada M. W., Vickroy T. W. and Kennedy R. T. ( 1997 ) High temporal resolution monitoring of glutamate and aspartate in vivo using microdialysis on‐line with capillary electrophoresis with laser‐induced fluorescence detection. Anal. Chem. 69, 4560 – 4565.en_US
dc.identifier.citedreferenceLai Y. Y. and Siegel J. M. ( 1988 ) Medullary regions mediating atonia. J. Neurosci. 8, 4790 – 4796.en_US
dc.identifier.citedreferenceLai Y. Y. and Siegel J. M. ( 1991 ) Pontomedullary glutamate receptors mediating locomotion and muscle tone suppression. J. Neurosci. 11, 2931 – 2937.en_US
dc.identifier.citedreferenceLai Y. Y., Clements J. R. and Siegel J. M. ( 1993 ) Glutamatergic and cholinergic projections to the pontine inhibitory area identified with horseradish peroxidase retrograde transport and immunohistochemistry. J. Comp. Neurol. 336, 321 – 330.en_US
dc.identifier.citedreferenceLéna I., Parrot S., Deschaux O., Muffat‐Joly S., Sauvinet V., Renaud B., Suaud‐Chagny M.‐F. and Gottesman C. ( 2005 ) Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep‐wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats. J. Neurosci. Res. 81, 891 – 899.en_US
dc.identifier.citedreferenceLeonard T. O. and Lydic R. ( 1997 ) Pontine nitric oxide modulates acetylcholine release, rapid eye movement sleep generation, and respiratory rate. J. Neurosci. 17, 774 – 785.en_US
dc.identifier.citedreferenceLiang C. L. and Marks G. A. ( 2009 ) A novel GABAergic afferent input to the pontine reticular formation: the mesopontine GABAergic column. Brain Res. 1297, 32 – 40.en_US
dc.identifier.citedreferenceLopez‐Rodriguez F., Medina‐Ceja L., Wilson C. L., Jhung D. and Morales‐Villagran A. ( 2007 ) Changes in extracellular glutamate levels in rat orbitofrontal cortex during sleep and wakefulness. Arch. Med. Res. 38, 52 – 55.en_US
dc.identifier.citedreferenceLydic R. and Baghdoyan H. A. ( 2002 ) Ketamine and MK‐801 decrease acetylcholine release in the pontine reticular formation, slow breathing, and disrupt sleep. Sleep 25, 617 – 622.en_US
dc.identifier.citedreferenceLydic R. and Baghdoyan H. A. ( 2008 ) Acetylcholine modulates sleep and wakefulness: a synaptic perspective, in Neurochemistry of Sleep and Wakefulness ( Monti J. M., Pandi‐Perumal S. R. and Sinton C. M., eds), pp. 109 – 143. Cambridge Univeristy Press, Cambridge, NY.en_US
dc.identifier.citedreferenceMallick B. N., Kaur S. and Saxena R. N. ( 2001 ) Interactions between cholinergic and GABAergic neurotransmitters in and around the locus coeruleus for the induction and maintenance of rapid eye movement sleep in rats. Neuroscience 104, 467 – 485.en_US
dc.identifier.citedreferenceMarks G. A., Sachs O. W. and Birabil C. G. ( 2008 ) Blockade of GABA, type A, receptors in the rat pontine reticular formation induces rapid eye movement sleep that is dependent upon the cholinergic system. Neuroscience 156, 1 – 10.en_US
dc.identifier.citedreferenceNitz D. and Siegel J. M. ( 1996 ) GABA release in posterior hypothalamus across sleep‐wake cycle. Am. J. Physiol. 271, R1707 – R1712.en_US
dc.identifier.citedreferenceNitz D. and Siegel J. ( 1997a ) GABA release in the dorsal raphe nucleus: role in the control of REM sleep. Am. J. Physiol. 273, R451 – R455.en_US
dc.identifier.citedreferenceNitz D. and Siegel J. M. ( 1997b ) GABA release in the locus coeruleus as a function of sleep/wake state. Neuroscience 78, 795 – 801.en_US
dc.identifier.citedreferencePal D. and Mallick B. N. ( 2009 ) GABA in pedunculopontine tegmentum increases rapid eye movement sleep in freely moving rats: possible role of GABA‐ergic inputs from substantia nigra pars reticulata. Neuroscience 164, 404 – 414.en_US
dc.identifier.citedreferencePaxinos G. and Watson C. ( 2007 ) The Rat Brain in Stereotaxic Coordinates, 6th edn. Academic Press, New York.en_US
dc.identifier.citedreferencePettit H. O. and Justice J. B. ( 1989 ) Dopamine in the nucleus accumbens during cocaine self‐administration as studied by in vivo microdialysis. Pharmacol. Biochem. Behav. 34, 899 – 904.en_US
dc.identifier.citedreferenceRodrigo‐Angulo M. L., Heredero S., Rodriguez‐Veiga E. and Reinoso‐Suarez F. ( 2008 ) GABAergic and non‐GABAergic thalamic, hypothalamic and basal forebrain projections to the ventral oral pontine reticular nucleus: their implication in REM sleep modulation. Brain Res. 1210, 116 – 125.en_US
dc.identifier.citedreferenceSanford L. D., Tang X., Xiao J., Ross R. J. and Morrison A. R. ( 2003 ) GABAergic regulation of REM sleep in reticularis pontis oralis and caudalis in rats. J. Neurophysiol. 90, 938 – 945.en_US
dc.identifier.citedreferenceSapin E., Lapray D., Berod A. et al. ( 2009 ) Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS ONE 4, e4272.en_US
dc.identifier.citedreferenceShackman J. G., Watson C. J. and Kennedy R. T. ( 2004 ) High‐throughput automated post‐processing of separation data. J. Chromatogr. A 1040, 273 – 282.en_US
dc.identifier.citedreferenceSimon C., Wallace‐Huitt T., Thapa P., Skinner R. D. and Garcia‐Rill E. ( 2011 ) Effects of glutamate receptor agonists on the p13 auditory evoked potential and startle response in the rat. Front. Neurol. 2, 3.en_US
dc.identifier.citedreferenceSmith A., Watson C. J., Frantz K. J., Eppler B., Kennedy R. T. and Peris J. ( 2004 ) Differential increase in taurine levels by low‐dose ethanol in the dorsal and ventral striatum revealed by microdialysis with on‐line capillary electrophoresis. Alcohol. Clin. Exp. Res. 28, 1028 – 1038.en_US
dc.identifier.citedreferenceStevens D. R., McCarley R. W. and Greene R. W. ( 1992 ) Excitatory amino acid‐mediated responses and synaptic potentials in medial pontine reticular formation neurons of the rat in vitro. J. Neurosci. 12, 4188 – 4194.en_US
dc.identifier.citedreferenceVanini G., Torterolo P., McGregor R., Chase M. H. and Morales F. R. ( 2007 ) GABAergic processes in the mesencephalic tegmentum modulate the occurrence of active (rapid eye movement) sleep in guinea pigs. Neuroscience 145, 1157 – 1167.en_US
dc.identifier.citedreferenceVanini G., Watson C. J., Lydic R. and Baghdoyan H. A. ( 2008 ) Gamma‐aminobutyric acid‐mediated neurotransmission in the pontine reticular formation modulates hypnosis, immobility, and breathing during isoflurane anesthesia. Anesthesiology 109, 978 – 988.en_US
dc.identifier.citedreferenceVanini G., Wathen B. L., Lydic R. and Baghdoyan H. A. ( 2011 ) Endogenous GABA levels in the pontine reticular formation (PRF) are greater during wakefulness than during REM sleep. J. Neurosci. 31, 2649 – 2656.en_US
dc.identifier.citedreferenceWatson C. J., Venton B. J. and Kennedy R. T. ( 2006 ) In vivo measurements of neurotransmitters by microdialysis sampling. Anal. Chem. 78, 1391 – 1399.en_US
dc.identifier.citedreferenceWatson C. J., Lydic R. and Baghdoyan H. A. ( 2007 ) Sleep and GABA levels in the oral part of rat pontine reticular formation are decreased by local and systemic administration of morphine. Neuroscience 144, 375 – 386.en_US
dc.identifier.citedreferenceWatson C. J., Lydic R. and Baghdoyan H. A. ( 2008 ) Pontine reticular formation (PnO) administration of hypocretin‐1 increases PnO GABA levels and wakefulness. Sleep 31, 453 – 464.en_US
dc.identifier.citedreferenceWigren H. K., Schepens M., Matto V., Stenberg D. and Porkka‐Heiskanen T. ( 2007 ) Glutamatergic stimulation of the basal forebrain elevates extracellular adenosine and increases the subsequent sleep. Neuroscience 147, 811 – 823.en_US
dc.identifier.citedreferenceXi M.‐C., Morales F. R. and Chase M. H. ( 1999 ) Evidence that wakefulness and REM sleep are controlled by a GABAergic pontine mechanism. J. Neurophysiol. 82, 2015 – 2019.en_US
dc.identifier.citedreferencevan der Zeyden M., Oldenziel W. H., Rea K., Cremers T. I. and Westerink B. H. ( 2008 ) Microdialysis of GABA and glutamate: analysis, interpretation and comparison with microsensors. Pharmacol. Biochem. Behav. 90, 135 – 147.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
j.1471-4159.2011.07350.x.pdf
Size:
442.5KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.