Maturation of sleep homeostasis in developing rats: A role for preoptic area neurons

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 4, 2011, Pages

  Gvilia, Irma ^a,b,c   Suntsova, Natalia ^b   Angara, Bryan ^a   McGinty, Dennis ^a,b   Szymusiak, Ronald ^a,b  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ILIA STATE UNIVERSITY   (Georgia)

Author keywords

Postnatal development; Preoptic hypothalamus; Sleep homeostasis; Sleep promoting systems

Indexed keywords

GLUTAMATE DECARBOXYLASE; PROTEIN C FOS;

ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; FEMALE; GABAERGIC SYSTEM; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NONREM SLEEP; PERINATAL PERIOD; PREOPTIC AREA; PRIORITY JOURNAL; RAT; REM SLEEP; SLEEP DEPRIVATION; THALAMUS VENTRAL NUCLEUS;

AGING; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; ELECTROENCEPHALOGRAPHY; GLUTAMIC ACID; HOMEOSTASIS; MODELS, ANIMAL; NEURONS; PREOPTIC AREA; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; SLEEP; SLEEP, REM; WAKEFULNESS;

EID: 79954465566     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00727.2010     Document Type: Article

References (50)

1. Alfoldi P, Tobler I, Borbely AA. Sleep regulation in rats during early development. Am J Physiol Regul Integr Comp Physiol 258: R634-R644, 1990.
2. Basheer R, Sherin JE, Saper CB, Morgan JI, McCarley RW, Shiromani PJ. Effects of sleep on wake-induced c-fos expression. J Neurosci 17: 9746-9750, 1997.
3. Bendova Z, Sumova A, Illnerova H. Development of circadian rhythmicity and photoperiodic response in subdivisions of the rat suprachiasmatic nucleus. Dev Brain Res 148: 105-112, 2004.
4. Berridge CW, Waterhouse BD. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42: 33-84, 2003.
5. Blumberg MS, Middlemis-Brown JE, Johnson ED. Sleep Homeostasis in Infant Rats. Behav Neurosci 118: 1253-1261, 2004.
6. Blumberg MS, Seelke MA, Lowen SB, Karlsson KE. Dynamics of sleep-wake cyclicity in developing rats. Proc Natl Acad Sci USA 102: 14860-14864, 2005.
7. Borbely AA, Tobler I. Homeostatic and circadian principals in sleep regulation in the rat. In: Brain Mechanisms of Sleep, edited by McGinty D. New York, NY: Raven, 1985.
8. Chou TC, Bjorkum AA, Gaus SE, Lu J, Scammell TE, Saper CB. Afferents to the ventrolateral preoptic nucleus. J Neurosci 22: 977-990, 2002.
9. Coyle JT, Yamamura HI. Neurochemical aspects of the ontogenesis of cholinergic neurons in the rat brain. Brain Res 118: 429-440, 1976.
10. Dragunow M, Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29: 261-265, 1989.
11. Fadel J, Sarter M, Bruno JP. Age-related attenuation of stimulated cortical acetylcholine release in basal forebrain-lesioned rats. Neurosci 90: 793-802, 1999.
12. Foote SL, Morrison JH. Development of the noradrenergic, serotonergic, and dopaminergic innervation of neocortex. Curr Top Dev Biol 21: 391-423, 1987.
13. Frank MG, Heller HC. Development of diurnal organization of EEG slow activity and slow wave sleep in the rat. Am J Physiol Regul Integr Comp Physiol 273: R472-R478, 1997.
14. Frank M, Morrissette R, Heller CH. Effects of sleep deprivation in neonatal rats. Am J Physiol Regul Integr Comp Physiol 275: R148-R157, 1998.
15. Franken P, Dijk DJ, Tobler I, Borbely AA. Sleep deprivation in the rat: effects on EEG power spectra, vigilance states, and cortical temperature. Am J Physiol Regul Integr Comp Physiol 261: R198-R208, 1991.
16. Gaus SE, Strecker RE, Tate BA, Parker RA, Saper CB. Ventrolateral preoptic nucleus contains sleep-active, galaninergic neurons in multiple mammalian species. Neuroscience 115: 285-294, 2002.
17. Geiger JD, LaBella FS, Nagy JI. Ontogenesis of adenosine receptors in the central nervous system of the rat. Brain Res 315: 97-104, 1984.
18. Giovannelli L, Shiromani PJ, Jirikowski GF, Bloom FE. Expression of c-fos protein by immunohistochemically identified oxytocin neurons in the rat hypothalamus upon osmotic stimulation. Brain Res 588: 41-48, 1992.
19. Gong H, Szymusiak R, King J, Steininger T, McGinty D. Sleep-related c-Fos protein expression in the preoptic hypothalamus: effects of ambient warming. Am J Physiol Regul Integr Comp Physiol 279: R2079-R2088, 2000.
20. Gong H, McGinty D, Guzman-Marin R, Chew KT, Stewart D, Szymusiak R. Activation of c-fos in GABAergic neurons in the preoptic area during sleep and in response to sleep deprivation. J Physiol (Lond) 556: 935-946, 2004.
21. Gramsbergen A, Schwartze P, Prechtl HF. The postnatal development of behavioral states in the rat. Dev Psychobiol 3: 267-280, 1970.
22. Gramsbergen A. The development of the EEG in the rat. Dev Psychobiol 9: 501-515, 1976.
23. Gvilia I, Turner A, McGinty D, Szymusiak R. Preoptic area neurons and the homeostatic regulation of rapid eye movement sleep. J Neurosci 26: 3037-3044, 2006.
24. Gvilia I, Szymusiak R. Regulation of nonREM Sleep: Interactions Among Sleep-Active Neurons in the Preoptic Hypothalamus. In: Current Advances in Sleep Biology: Regulation and Function, edited by Frank M. New York, NY: Nova Science, 2010.
25. Gvilia I, Xu F, McGinty D, Szymusiak R. Homeostatic regulation of sleep: a role for preoptic area neurons. J Neurosci 26: 9426-9433, 2006.
26. Ibuka N. Ontogenesis of circadian sleep-wakefulness rhythms and developmental changes of sleep in the altricial rat and in the precocial guinea pig. Behav Brain Res 11: 185-196, 1984.
27. Imaki T, Shibasaki T, Hotta M, Demura H. Early induction of c-fos precedes increased expression of corticotropin-releasing factor messenger ribonucleic acid in the paraventricular nucleus after immobilization stress. Endocrinology 131: 240-246, 1992.
28. Karlsson KE, Kreider JC, Blumberg MS. Hypothalamic contribution to sleep-wake cycle development. Neuroscience 123: 575-582, 2004.
29. Kleitman N, Engelmann TG. Sleep characteristics of infants. J Appl Physiol 6: 269-282, 1953.
30. Kovacikova Z, Sladek M, Laurinova K, Bendova Z, Illnerova H, Sumova A. Ontogenesis of photoperiodic entrainment of the molecular core clockwork in the rat suprachiasmatic nucleus. Brain Res 1064: 83-89, 2005.
31. Leard LE, Macdonald ES, Heller HC, Kilduff TS. Ontogeny of photicinduced c-fos mRNA expression in rat suprachiasmatic nuclei. NeuroReport 5: 2683-2687, 1994.
32. Levitt P, Moore RY. Development of the noradrenergic innervation of neocortex. Brain Res 162: 243-259 1979.
33. Maloney KJ, Cape EG, Gotman J, Jones BE. High-frequency electroencephalogram activity in association with sleep-wake states and spontaneous behaviors in the rat. Neuroscience 76: 541-55 1997.
34. Mistlberger RE. Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res Rev 49: 429-454, 2005.
35. Miyata S, Itoh T, Lin SH, Ishiyama M, Nakashima T, Kiyohara T. Temporal changes of c-fos expression in oxytocinergic magnocellular neuroendocrine cells of the rat hypothalamus with restraint stress. Brain Res Bull 37: 391-395, 1995.
36. Mohns EJ, Karlsson KA, Blumberg MS. The preoptic hypothalamus and basal forebrain play opposing roles in the descending modulation of sleep and wakefulness in infant rats. Eur J Neurosci 23: 1301-1310, 2006.
37. Morgan JI, Curran T. Role of ion flux in the control of c-fos expression. Nature 322: 552-555, 1986.
38. Saper CB, Cano G, Scammell TE. Homeostatic, circadian, and emotional regulation of sleep. J Comp Neurol 493: 477-478, 2005.
39. Sawai N, Ueta Y, Nakazato M, Ozava H. Developmental and aging changes of orexin-A and-B immunoreactive neurons in the mail rat hypothalamus. Neurosci Lett 468: 51-55, 2010.
40. Seelke AM, Blumberg MS. The microstructure of active and quiet sleep as cortical delta activity emerges in infant rats. Sleep 31: 691-699, 2008.
41. Sherin JE, Elmquist JK, Torrealba F, Saper CB. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 18: 4705-4721, 1998.
42. Shiromani PJ, Malik M, Winston S, McCarley RW. Time course of Fos-like immunoreactivity associated with cholinergically induced REM sleep. J Neurosci 15: 3500-3508, 1995.
43. Sim LJ, Morris M. Fos activation in cultured tyrosine hydroxylase and oxytocin immunoreactive neurons. Brain Res Bull 36: 399-404, 1995.
44. Suntsova N, Szymusiak R, Alam MN, Guzman-Marin R, McGinty D. Sleep-waking discharge patterns of median preoptic nucleus neurons in rats. J Physiol (Lond) 543: 665-667, 2002.
45. Szymusiak R, Alam MN, Steininger TL, McGinty D. Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Res 803: 178-188, 1998.
46. Szymusiak R, Gvilia I, McGinty D. Hypothalamic Control of Sleep. Sleep Med 8: 291-301, 2007.
47. Todd WD, Gibson JL, Shaw CS, Blumberg MS. Brainstem and hypothalamic regulation of sleep pressure and rebound in newborn rats. Behav Neurosci 124: 69-78, 2010.
48. Uschakov A, Gong H, McGinty D, Szymusiak R. Sleep-active neurons in the preoptic area project to the hypothalamic paraventricular nucleus and the perifornical lateral hypothalamus. Eur J Neurosci 23: 3284-3296, 2006.
49. Uschakov A, Gong H, McGinty D, Szymusiak R. Efferent projections from the median preoptic nucleus to sleep-and arousal-regulatory nuclei in the rat brain. Neuroscience 150: 104-120, 2007.
50. Valatx JL, Jouvet M. Circadian rhythms of slow-wave sleep and paradoxical sleep are in opposite phase in genetically hypoprolactinemic rats. C R Acad Sci III 307: 789-794, 1988.