Skip to main content Accessibility help
×
Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-07T22:18:13.925Z Has data issue: false hasContentIssue false

16 - Hippocampal theta rhythm of REM sleep

from Section III - Neuronal regulation

Published online by Cambridge University Press:  07 September 2011

Robert P. Vertes
Affiliation:
Florida Atlantic University
Birendra N. Mallick
Affiliation:
Jawaharlal Nehru University
S. R. Pandi-Perumal
Affiliation:
Somnogen Canada Inc, Toronto
Robert W. McCarley
Affiliation:
Harvard University, Massachusetts
Adrian R. Morrison
Affiliation:
University of Pennsylvania
Get access

Summary

Summary

The theta rhythm of the hippocampus is a large- amplitude (1–2 mV), nearly sinusoidal oscillation of 5 to 12 Hz. Theta is present in the hippocampus of the rat during the exploratory movements of waking and continuously throughout REM sleep. In early reports, we identified neurons of the nucleus pontis oralis (RPO) of the pons that discharged in association with the theta of waking and REM sleep, and subsequently showed that electrical stimulation or carbachol injections into the RPO very effectively elicited theta. These findings indicated that RPO was the brain-stem source for the generation of theta. In related studies, we described an ascending RPO to septohippocampal system routed through the hypothalamic supramammillary nucleus controlling theta, and further demonstrated that the serotonin-containing median raphe (MR) nucleus desynchronized the hippocampal EEG – or blocked theta. The latter indicates that theta, like other events of REM sleep, is subject to aminergic modulation; that is, the suppression of MR activity during REM releases theta in that state. Theta serves a well recognized role in memory processing in waking. We suggest that theta does not serve the same function in REM sleep (memory processing), but rather theta (of REM) is a by-product of the intense forebrain activation of REM sleep, which serves the important function of maintaining the minimum requisite levels of activity periodically throughout sleep to ensure and promote recovery from sleep.

Type
Chapter
Information
Rapid Eye Movement Sleep
Regulation and Function
, pp. 151 - 163
Publisher: Cambridge University Press
Print publication year: 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, K. L., Rajagovindan, R., Ghacibeh, G. A., Meador, K. J. & Ding, M. (2009) Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb Cortex, Epub 2009 Oct 27.Google ScholarPubMed
Assaf, S. Y. & Miller, J. J. (1978) Role of a raphe serotonin system in control of septal unit-activity and hippocampal desynchronization. Neuroscience 3: –50.CrossRefGoogle ScholarPubMed
Bland, B. H. (1986) The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26: –54.CrossRefGoogle ScholarPubMed
Bland, B. H., Oddie, S. D., Colom, L. V. & Vertes, R. P. (1994) The extrinsic modulation of medial septal cell discharges by the ascending brainstem hippocampal synchronizing pathway. Hippocampus 4: –60.CrossRefGoogle ScholarPubMed
Bland, B. H., Konopacki, J., Kirk, I. J., Oddie, S. D. & Dickson, C. T. (1995) Discharge patterns of hippocampal theta-related cells in the caudal diencephalon of the urethane-anesthetized rat. J Neurophysiol 74: –33.CrossRefGoogle Scholar
Buzsaki, G. (2002) Theta oscillations in the hippocampus. Neuron 33: –40.CrossRefGoogle ScholarPubMed
Datta, S. & Maclean, R. R. (2007) Neurobiological mechanisms for the regulation of mammalian sleep-wake behavior: reinterpretation of historical evidence and inclusion of contemporary cellular and molecular evidence. Neurosci Biobehav Rev 31: –824.CrossRefGoogle ScholarPubMed
Diekelmann, S., Wilhelm, I. & Born, J. (2009) The whats and whens of sleep-dependent memory consolidation. Sleep Med Rev 13: –21.CrossRefGoogle ScholarPubMed
Forchetti, C. M. & Meek, J. L. (1981) Evidence for a tonic GABAergic control of serotonin neurons in the median raphe nucleus. Brain Res 206: –12.CrossRefGoogle ScholarPubMed
Green, J. D. & Arduini, A. A. (1954) Hippocampal electrical activity in arousal. J Neurophysiol 17: –57.CrossRefGoogle ScholarPubMed
Hobson, J. A., McCarley, R. W., Pivik, R. T. & Freedman, R. (1974) Selective firing by cat pontine brain stem neurons in desynchronized sleep. J Neurophysiol 37: –511.Google ScholarPubMed
Hobson, J. A., McCarley, R. W., Wyzinski, P. W. (1975) Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189: –8.CrossRefGoogle ScholarPubMed
Jackson, J., Dickson, C.T. & Bland, B. H. (2008) Median raphe stimulation disrupts hippocampal theta via rapid inhibition and state-dependent phase reset of theta-related neural circuitry. J Neurophysiol 99: –26.CrossRefGoogle ScholarPubMed
Jacobs, B. L. & Azmitia, E. C. (1992) Structure and function of the brain serotonin system. Physiol Rev 72: –229.CrossRefGoogle ScholarPubMed
Jarosiewicz, B. & Skaggs, W. E. (2004) Level of arousal during the small irregular activity state in the rat hippocampal EEG. J Neurophysiol 91: –57.CrossRefGoogle Scholar
Kinney, G. G., Kocsis, B. & Vertes, R. P. (1994) Injections of excitatory amino acid antagonists into the median raphe nucleus produce hippocampal theta rhythm in the urethane anesthetized rat. Brain Res 654: –104.CrossRefGoogle ScholarPubMed
Kinney, G. G., Kocsis, B. & Vertes, R. P. (1995) Injections of muscimol into the median raphe nucleus produce hippocampal theta rhythm in the urethane anesthetized rat. Psychopharmacology 120: –48.CrossRefGoogle ScholarPubMed
Kinney, G. G., Kocsis, B. & Vertes, R. P. (1996) Medial septal unit firing characteristics following injections of 8-OH-DPAT into the median raphe nucleus. Brain Res 708: –22.CrossRefGoogle ScholarPubMed
Kirk, I. J. & McNaughton, N. (1991) Supramammillary cell firing and hippocampal rhythmical slow activity. Neuroreport 2: –5.CrossRefGoogle ScholarPubMed
Kitchigina, V. F., Kudina, T. A., Kutyreva, E. V. & Vinogradova, O. S. (1999) Neuronal activity of the septal pacemaker of theta rhythm under the influence of stimulation and blockade of the median raphe nucleus in the awake rabbit. Neuroscience 94: –63.CrossRefGoogle ScholarPubMed
Kocsis, B., Varga, V., Dahan, L. & Sik, A. (2006) Serotonergic neuron diversity: identification of raphe neurons with discharges time-locked to the hippocampal theta rhythm. Proc Natl Acad Sci USA 103: –64.CrossRefGoogle ScholarPubMed
Kocsis, B. & Vertes, R. P. (1994) Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J Neurosci 14: –52.CrossRefGoogle ScholarPubMed
Kocsis, B. & Vertes, R. P. (1996) Midbrain raphe cell firing and hippocampal theta rhythm in urethane anaesthetized rats. Neuroreport 7: –72.CrossRefGoogle ScholarPubMed
Kudina, T. A., Sudnitsyn, V. V., Kutyreva, E. V. & Kichigina, V. F. (2004) The serotonin reuptake inhibitor fluoxetine suppresses theta oscillations in the electroencephalogram of the rabbit hippocampus. Neurosci Behav Physiol 34: –33.CrossRefGoogle ScholarPubMed
Luppi, P. H., Gervasoni, D., Verret, L. . (2007) Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J Physiol (Paris) 100: –83.Google Scholar
Maloney, K. J., Mainville, L. & Jones, B. E. (1999) Differential c-Fos expression in cholinergic, monoaminergic, and GABAergic cell groups of the pontomesencephalic tegmentum after paradoxical sleep deprivation and recovery. J Neurosci 19: –72.CrossRefGoogle ScholarPubMed
Maru, E., Takahashi, L. K. & Iwahara, S. (1979) Effects of median raphe nucleus lesions on hippocampal EEG in the freely moving rat. Brain Res 163: –34.CrossRefGoogle ScholarPubMed
McCarley, R. W. & Hobson, J. A. (1971) Single neuron activity in cat gigantocellular tegmental field: selectivity of discharge in desynchronized sleep. Science 174: –2.CrossRefGoogle ScholarPubMed
Morin, L.P. & Meyer-Bernstein, E. L. (1999) The ascending serotonergic system in the hamster: comparison with projections of the dorsal and median raphe nuclei. Neuroscience 91: –105.CrossRefGoogle ScholarPubMed
Nũnez, A., de Andrés, I. & García-Austt, E. (1991) Relationships of nucleus reticularis pontis oralis neuronal discharge with sensory and carbachol evoked hippocampal theta rhythm. Exp Brain Res 87: –8.CrossRefGoogle ScholarPubMed
Pan, W. X. & McNaughton, N. (2004) The supramammillary area: its organization, functions and relationship to the hippocampus. Prog Neurobiol 74: –66.CrossRefGoogle ScholarPubMed
Petsche, H., Gogolak, G. & Vanzwiet, P. A. (1965) Rhythmicity of septal cell discharges at various levels of reticular excitation. Electroenceph Clin Neurophysiol 19: –33.CrossRefGoogle ScholarPubMed
Rasch, B., Pommer, J., Diekelmann, S. & Born, J. (2009) Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat Neurosci 12: –7.CrossRefGoogle ScholarPubMed
Rickard, T. C., Cai, D. J., Rieth, C. A., Jones, J. & Ard, M. C. (2008) Sleep does not enhance motor sequence learning. J Exp Psychol Learn Mem Cogn 34: –42.CrossRefGoogle Scholar
Sakai, K. & Jouvet, M. (1980) Brain stem PGO-on cells projecting directly to the cat dorsal lateral geniculate nucleus. Brain Res 194: –5.CrossRefGoogle ScholarPubMed
Siegel, J. M. (2001) The REM sleep-memory consolidation hypothesis. Science 294: –63.CrossRefGoogle ScholarPubMed
Siegel, J. M., McGinty, D. J. & Breedlove, S. M. (1977) Sleep and waking activity of pontine gigantocellular field neurons. Exp Neurol 56: –73.CrossRefGoogle ScholarPubMed
Song, S., Howard, J. H. & Howard, D. V. (2007) Sleep does not benefit probabilistic motor sequence learning. J Neurosci 27: –83.CrossRefGoogle Scholar
Takano, Y. & Hanada, Y. (2009) The driving system for hippocampal theta in the brainstem: an examination by single neuron recording in urethane-anesthetized rats. Neurosci Lett 455: –9.CrossRefGoogle ScholarPubMed
Urbain, N., Creamer, K. & Debonnel, G. (2006) Electrophysiological diversity of the dorsal raphe cells across the sleep–wake cycle of the rat. J Physiol 573: –95.CrossRefGoogle ScholarPubMed
Vanderwolf, C. H. (1971) Limbic-diencephalic mechanisms of voluntary movement. Psychol Rev 78: –113.CrossRefGoogle ScholarPubMed
Varga, V., Sik, A., Freund, T. F. & Kocsis, B. (2002) GABA(B) receptors in the median raphe nucleus: distribution and role in the serotonergic control of hippocampal activity. Neuroscience 109: –32.CrossRefGoogle ScholarPubMed
Vertes, R. P. (1977) Selective firing of rat pontine gigantocellular neurons during movement and REM sleep. Brain Res 128: –52.CrossRefGoogle ScholarPubMed
Vertes, R. P. (1979) Brain stem gigantocellular neurons: patterns of activity during behavior and sleep in the freely moving rat. J Neurophysiol 42: –28.CrossRefGoogle ScholarPubMed
Vertes, R. P. (1981) An analysis of ascending brain stem systems involved in hippocampal synchronization and desynchronization. J Neurophysiol 46: –59.CrossRefGoogle ScholarPubMed
Vertes, R. P. (1982) Brain stem generation of the hippocampal EEG. Prog Neurobiol 19: –86.CrossRefGoogle ScholarPubMed
Vertes, R. P. (1984) Brainstem control of the events of REM sleep. Prog Neurobiol 22: –88.CrossRefGoogle ScholarPubMed
Vertes, R. P. (1986) A life-sustaining function for REM sleep: a theory. Neurosci Biobehav Rev 10: –6.CrossRefGoogle ScholarPubMed
Vertes, R. P. (1988) Brainstem afferents to the basal forebrain in the rat. Neuroscience 24: –35.CrossRefGoogle ScholarPubMed
Vertes, R. P. (1990) Brainstem mechanisms of slow wave sleep and REM sleep. In Brainstem Mechanisms of Behavior, eds. R. P. Vertes & W. R. Klemm. New York:John Wiley & Sons, pp. 535–83.Google Scholar
Vertes, R. P. (1992) PHA-L analysis of projections from the supramammillary nucleus in the rat. J Comp Neur 326: –622.CrossRefGoogle ScholarPubMed
Vertes, R. P. (2004) Memory consolidation in sleep: dream or reality. Neuron 44: –48.CrossRefGoogle ScholarPubMed
Vertes, R. P. (2005) Hippocampal theta rhythym: a tag for short-term memory. Hippocampus 15: –35.CrossRefGoogle Scholar
Vertes, R. P. & Martin, G. F. (1988) Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. J Comp Neurol 275: –41.CrossRefGoogle ScholarPubMed
Vertes, R. P. & Kocsis, B. (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81: –926.Google ScholarPubMed
Vertes, R. P. & Eastman, K. E. (2000) The case against memory consolidation in REM sleep. Behav Brain Sci 23: –76.CrossRefGoogle ScholarPubMed
Vertes, R. P. & Siegel, J. M. (2005) Time for the sleep community to take a critical look at the purported role of sleep in memory processing. Sleep 28:–9.CrossRefGoogle Scholar
Vertes, R. P. & Linley, S. B. (2007) Comparisons of projections of the dorsal and median raphe nuclei, with some functional considerations. In , ed. Takai, K.. International Congress Series, 1304, pp. 98–120.CrossRef
Vertes, R. P., Colom, L. V., Fortin, W. J. & Bland, B. H. (1993) Brainstem sites for the carbachol elicitation of the hippocampal theta rhythm in the rat. Exp Brain Res 96: –29.CrossRefGoogle ScholarPubMed
Vertes, R. P., Kinney, G. G., Kocsis, B. & Fortin, W. J. (1994) Pharmacological suppression of the median raphe nucleus with serotonin1A agonists, 8-OH-DPAT and buspirone, produces hippocampal theta-rhythm in the rat. Neuroscience 60: –51.CrossRefGoogle ScholarPubMed
Vertes, R. P., Fortin, W. J. & Crane, A. M. (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407: –82.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Vertes, R. P., Hoover, W.B. & Viana Di Prisco, G. (2004) Theta rhythm of the hippocampus: subcortical control and functional significance. Behav Cogn Neurosci Rev 3: –200.CrossRefGoogle ScholarPubMed
Viana Di Prisco, G., Albo, Z., Vertes, R. P. & Kocsis, B. (2002) Discharge properties of neurons of the median raphe nucleus during hippocampal theta rhythm in the rat. Exp Brain Res 145: –94.CrossRefGoogle ScholarPubMed
Vinogradova, O. S., Kitchigina, V. F., Kudina, T. A. & Zenchenko, K. I. (1999) Spontaneous activity and sensory responses of hippocampal neurons during persistent theta-rhythm evoked by median raphe nucleus blockade in rabbit. Neuroscience 94: –53.CrossRefGoogle ScholarPubMed
Walker, M. P. & Stickgold, R. (2004) Sleep-dependent learning and memory consolidation. Neuron 44: –33.CrossRefGoogle ScholarPubMed
Yamamoto, T., Watanabe, S., Oishi, R. & Ueki, S. (1979) Effects of midbrain raphe stimulation and lesion on EEG activity in rats. Brain Res Bull 4: –5.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×