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32 - Sleep-related hippocampal activation: implications for spatial memory consolidation

from Section V - Functional significance

Published online by Cambridge University Press:  07 September 2011

Dinesh Pal
Affiliation:
University of Michigan
Victoria Booth
Affiliation:
University of Michigan
Gina R. Poe
Affiliation:
University of Michigan
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
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Summary

Summary

Sleep is implicated in the consolidation of many types of learning and memory tasks. Place cells (hippocampal neurons responding to spatial location of the subject) associated with novel environments on a spatial task reactivate during subsequent sleep (Poe et al., 2000). Such neuronal firing is thought to strengthen memories formed during waking exploration (Huerta and Lisman, 1995). Once the initially novel environment becomes familiar to the animal, place cells reverse phase at which they fire with respect to local theta oscillations during REM sleep. Such phase-reversed firing during theta is consistent with patterns that induce the depotentiation of previously potentiated synapses. Depotentiation is important to prevent the saturation of synaptic weights in the hippocampus, keeping the differential weighting structure necessary for memory preservation. These results indicate that sleep in general seems to serve neither an overall synaptic erasing (Tononi and Cirelli, 2001) nor a general synaptic amplification effect. Rather, in a network-by-network manner (Ribeiro and Nicolelis, 2004) and, according to the requirements of the learning phase, REM-sleep reactivation serves to amplify as-yet-unconsolidated memories and erase already transferred networks from the temporary stores of the hippocampus (Best et al., 2007; Booth and Poe, 2006).

Type
Chapter
Information
Rapid Eye Movement Sleep
Regulation and Function
, pp. 319 - 327
Publisher: Cambridge University Press
Print publication year: 2011

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References

Almaguer-Melian, W., Rojas-Reyes, Y., Alvare, A. . (2005) Long-term potentiation in the dentate gyrus in freely moving rats is reinforced by intraventricular application of norepinephrine, but not oxotremorine. Neurobiol Learn Mem 83: –8.CrossRefGoogle Scholar
Aston-Jones, G. & Bloom, F. E. (1981) Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep–waking cycle. J Neurosci 1: –86.CrossRefGoogle ScholarPubMed
Best, J., Diniz Behn, C., Poe, G.R. & Booth, V. (2007) Neuronal models for sleep–wake regulation and synaptic reorganization in the sleeping hippocampus. J Biol Rhythms 22: –32.CrossRefGoogle ScholarPubMed
Bjorness, T. E., Riley, B. T., Tysor, M. K. & Poe, G. R. (2005) REM restriction persistently alters strategy used to solve a spatial task. Learn Mem 12(3) –9.CrossRefGoogle ScholarPubMed
Blitzer, RD., Iyengar, R. & Landau, E.M. (2005) Postsynaptic signaling networks: cellular cogwheels underlying long-term plasticity. Biol Psych 57:–39.Google ScholarPubMed
Booth, V. & Poe, G. R. (2006). Input source and strength influences overall firing phase of model hippocampal CA1 pyramidal cells during theta: relevance to REM sleep reactivation and memory consolidation. Hippocampus 16: –73.CrossRefGoogle ScholarPubMed
Braunewell, K. H. & Manahan-Vaughan, D. (2001) Long-term depression: a cellular basis for learning?Rev Neurosci 12: –40.CrossRefGoogle ScholarPubMed
Buzsáki, G., Leung, L.W. & Vanderwolf, C.H. (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287: –71.Google ScholarPubMed
Campbell, I. G., Guinan, M. J. & Horowitz, J. M. (2002). Sleep deprivation impairs long-term potentiation in rat hippocampal slices. J Neurophysiol 88: –6.CrossRefGoogle ScholarPubMed
Corkin, S. (2002) What’s new with the amnesic patient H. M.?Nat Rev Neurosci 3: –60.CrossRefGoogle ScholarPubMed
Dave, A. S. & Margoliash, D. (2000) Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290: –16.CrossRefGoogle ScholarPubMed
Davis, C. J., Harding, J. W. & Wright, J. W. (2003) REM sleep deprivation-induced deficits in the latency-to-peak induction and maintenance of long-term potentiation within the CA1 region of the hippocampus. Brain Res 973: –7.CrossRefGoogle ScholarPubMed
Ekstrom, A. D., Meltzer, J., McNaughton, B. L. & Barnes, C. A. (2001) NMDA receptor antagonism blocks experience dependent expansion of hippocampal “place fields”. Neuron 31: –8.CrossRefGoogle ScholarPubMed
Fox, S. E., Wolfson, S. & Ranck, J. B. Jr. (1986). Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62: –508.CrossRefGoogle ScholarPubMed
Frank, M. G. & Benington, J. H. (2006) The role of sleep in memory consolidation and brain plasticity: dream or reality?Neuroscientist 12: –88.CrossRefGoogle ScholarPubMed
Gasparini, S. & DiFrancesco, D. (1999) Action of serotonin on the hyperpolarization-activated cation current (Ih) in rat CA1 hippocampal neurons. Eur J Neurosci 11: –100.CrossRefGoogle Scholar
Huerta, P. T. & Lisman, J. E. (1995). Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15: –63.CrossRefGoogle ScholarPubMed
Hyman, J. M., Wyble, B. P., Goyal, V., Rossi, C. A. & Hasselmo, M. E. (2003) Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23: –31.CrossRefGoogle ScholarPubMed
Jablonski, P., Poe, G. R. & Zochowski, M. (2007) Structural network heterogeneities and network dynamics: a possible dynamical mechanism for hippocampal memory reactivation. Phys Rev E Stat Nonlin Soft Matter Phys 75: .CrossRefGoogle ScholarPubMed
Karni, A., Tanne, D., Rubenstein, B. S., Askenasy, J. J. M. & Sagi, D. (1994) Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265: –82.CrossRefGoogle ScholarPubMed
Katsuki, H., Izumi, Y. & Zorumski, C. F. (1997) Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J Neurophysiol 77: –20.CrossRefGoogle Scholar
Kemp, A. & Manahan-Vaughan, D. (2004) Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci U S A 101: –7.CrossRefGoogle ScholarPubMed
Louie, K. & Wilson, M.A. (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29: –56.CrossRefGoogle ScholarPubMed
Lydic, R. & Baghdoyan, H. A. (1993) Pedunculopontine stimulation alters respiration and increases ACh release in the pontine reticular formation. Am J Physiol 264: –54.Google ScholarPubMed
Lydic, R., Baghdoyan, H. A. & Lorinc, Z. (1991) Microdialysis of cat pons reveals enhanced acetylcholine release during state-dependent respiratory depression. Am J Physiol 261: –70.Google ScholarPubMed
Manahan-Vaughan, D. & Braunewell, K. H. (1999). Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci U S A 96: –44.CrossRefGoogle ScholarPubMed
Marks, C. A. & Wayner, M. J. (2005) Effects of sleep disruption on rat dentate granule cell LTP in vivo. Brain Res Bull 66: –19.CrossRefGoogle ScholarPubMed
Martin, S. J., de Hoz, L. & Morris, R. G. (2005) Retrograde amnesia: neither partial nor complete hippocampal lesions in rats result in preferential sparing of remote spatial memory, even after reminding. Neuropsychologia 43: –24.CrossRefGoogle ScholarPubMed
McDermott, C. M., LaHoste, G. J., Chen, C., . (2003) Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. J Neurosci 23: –95.CrossRefGoogle ScholarPubMed
Mednick, S. C., Nakayama, K., Cantero, J. L., . (2002) The restorative effect of naps on perceptual deterioration. Nat Neurosci 5: –81.CrossRefGoogle ScholarPubMed
Mehta, M. R., Barnes, C. A. & McNaughton, B. L. (1997) Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci U S A 94: –21.CrossRefGoogle ScholarPubMed
Mehta, M. R., Quirk, M. C. & Wilson, M. A. (2000) Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25: –15.CrossRefGoogle ScholarPubMed
Meneses, A. & Hong, E. (1997) Effects of 5-HT4 receptor agonists and antagonists in learning. Pharmacol Biochem Behav 56: –51.CrossRefGoogle Scholar
Nakao, K., Ikegaya, Y., Yamada, M. K., Nishiyama, N. & Matsuki, N. (2002) Hippocampal long-term depression as an index of spatial working memory. Eur J Neurosci 16: –4.CrossRefGoogle ScholarPubMed
O’Keefe, J. & Dostrovsky, J. (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34: –5.Google ScholarPubMed
Ordy, J. M., Thomas, G. J., Volpe, B. T., Dunlap, W. P. & Colombo, P. M. (1988) An animal model of human-type memory loss based on aging, lesion, forebrain ischemia, and drug studies with the rat. Neurobiol Aging 9: –83.CrossRefGoogle ScholarPubMed
Pace-Schott, E. F. & Hobson, J. A. (2002) The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat Rev Neurosci 3: –605.CrossRefGoogle ScholarPubMed
Park, S. P., Lopez-Rodriguez, F., Wilson, C. L. . (1999) In vivo microdialysis measures of extracellular serotonin in the rat hippocampus during sleep–wakefulness. Brain Res 833: –6.CrossRefGoogle ScholarPubMed
Pavlides, C., Greenstein, Y. J., Grudman, M. & Winson, J. (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439: –7.CrossRefGoogle ScholarPubMed
Pavlides, C. & Winson, J. (1989) Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci 9: –18.CrossRefGoogle ScholarPubMed
Pedemonte, M., Barrenechea, C., Nuñez, A., Gambini, J. P. & García-Austt, E. (1998) Membrane and circuit properties of lateral septum neurons: relationships with hippocampal rhythms. Brain Res 800: –53.CrossRefGoogle ScholarPubMed
Poe, G. R., Nitz, D. A, McNaughton, B. L. & Barnes, C. A. (2000) Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res 855: –80.CrossRefGoogle ScholarPubMed
Rempel-Clower, N. L., Zola, S. M., Squire, L. R. & Amaral, D. G. (1996) Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J Neurosci 16: –55.CrossRefGoogle ScholarPubMed
Ribeiro, S., Mello, Nicolelis, , M. A. L. (2004) Reverberation, storage, and postsynaptic propagation of memories during sleep. Learn Mem 11: –96.CrossRefGoogle ScholarPubMed
Robinson, R. B. & Siegelbaum, S. A. (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Ann Rev Physiol 65: –80.CrossRefGoogle ScholarPubMed
Romcy-Pereira, R. & Pavlides, C. (2004) Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. Eur J Neurosci 20: –62.CrossRefGoogle ScholarPubMed
Sagar, H. J., Cohen, N. J., Corkin, S. & Growdon, J. H. (1985) Dissociations among processes in remote memory. Ann N Y Acad Sci 444: –5.CrossRefGoogle ScholarPubMed
Scoville, W. B. & Milner, B. (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psych 20: –21.CrossRefGoogle ScholarPubMed
Shapiro, M. (2001) Plasticity, hippocampal place cells, and cognitive maps. Arch Neurol 58: –81.CrossRefGoogle ScholarPubMed
Siapas, A. G., Lubenov, E. V. & Wilson, M. A. (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46: –51.CrossRefGoogle ScholarPubMed
Smith, C. (1996) Sleep states, memory processes and synaptic plasticity. Behav Brain Res 78: –56.CrossRefGoogle ScholarPubMed
Smith, C. & Rose, G. M. (1997) Posttraining paradoxical sleep in rats is increased after spatial learning in the Morris water maze. Behav Neurosci 111: –204.CrossRefGoogle ScholarPubMed
Squire, L. R. (2004) Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 82: –7.CrossRefGoogle ScholarPubMed
Steriade, M. & McCarley, R. W. (2007) Brain Stem Control of Wakefulness and Sleep. New York: Plenum.Google Scholar
Stickgold, R., Hobson, J. A., Fosse, R. & Fosse, M. (2001) Sleep, learning, and dreams: off-line memory reprocessing. Science 294: –7.CrossRefGoogle ScholarPubMed
Thomas, M. J., Moody, T. D., Makhinson, M. & O’Dell, T. J. (1996) Activity dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17: –82.CrossRefGoogle ScholarPubMed
Thompson, L. T. & Best, P. J. (1990) Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res 509: –308.CrossRefGoogle ScholarPubMed
Tononi, G. & Cirelli, C. (2001) Modulation of brain gene expression during sleep and wakefulness: a review of recent findings. Neuropsychopharmacology 25: –35.CrossRefGoogle ScholarPubMed
Vertes, R. P. & Kocsis, B. (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81: –926.Google ScholarPubMed
Volpe, B. T., Pulsinelli, W. A., Tribuna, J. & Davis, H. P. (1984) Behavioral performance of rats following transient forebrain ischemia. Stroke 15: –62.CrossRefGoogle ScholarPubMed
Walker, M. P. & Stickgold, R. (2004) Sleep-dependent learning and memory consolidation. Neuron 44: –33.CrossRefGoogle ScholarPubMed
Wang, J. X., Poe, G. & Zochowski, M. (2008) From network heterogeneities to familiarity detection and hippocampal memory management. Phys Rev E Stat Nonlin Soft Matter Phys 78: .CrossRefGoogle ScholarPubMed
Wierzynski, C. M., Lubenov, E. V., Gu, M. & Siapas, A. G. (2009) State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61: –96.CrossRefGoogle ScholarPubMed
Wilson, M. A. & McNaughton, B. L. (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265: –9.CrossRefGoogle ScholarPubMed
Xu, L., Anwyl, R. & Rowan, M. J. (1998) Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394: –4.CrossRefGoogle ScholarPubMed
Yang, H. W., Lin, Y. W., Yen, C. D. & Min, M. Y. (2002) Change in bi-directional plasticity at CA1 synapses in hippocampal slices taken from 6-hydroxydopamine-treated rats: the role of endogenous norepinephrine. Eur J Neurosci 16: –28.Google ScholarPubMed
Zola-Morgan, S., Squire, L. R. & Amaral, D. G. (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6: –67.CrossRefGoogle ScholarPubMed
Zola-Morgan, S., Squire, L. R. & Amaral, D. G. (1989) Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys. J Neurosci 9: –913.CrossRefGoogle ScholarPubMed
Zola-Morgan, S., Squire, L. R., Rempel, N. L., Clower, R. P. & Amaral, D. G. (1992) Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J Neurosci 12: –96.CrossRefGoogle ScholarPubMed

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