Visual–Procedural Memory Consolidation during Sleep Blocked by Glutamatergic Receptor Antagonists

Visual cortex plasticity is enhanced by sleep. It is hypothesized that a reactivation of glutamatergic synapses is essential for this form of plasticity to occur after learning. To test this hypothesis, human subjects practiced a visual texture discrimination skill known to require post-training sleep for improvements to occur. During sleep, glutamatergic transmission was inhibited by administration of the two glutamate antagonists, caroverine and ketamine, targeting the ionotropic NMDA and AMPA receptors. Both substances given during consolidation sleep in a placebo controlled crossover design were able to prevent improvement of the skill measured the next morning. An off-line activation of glutamatergic synapses therefore seems to play a critical part in the consolidation of plastic changes in the visual cortex.

[1]  J. Born,et al.  Odor Cues During Slow-Wave Sleep Prompt Declarative Memory Consolidation , 2007, Science.

[2]  Dov Sagi,et al.  A link between perceptual learning, adaptation and sleep , 2006, Vision Research.

[3]  W. Tischmeyer,et al.  Consolidation of auditory cortex-dependent memory requires N-methyl-d-aspartate receptor activation , 2006, Neuropharmacology.

[4]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

[5]  C. Degueldre,et al.  Offline Persistence of Memory-Related Cerebral Activity during Active Wakefulness , 2006, PLoS biology.

[6]  Tobias Bonhoeffer,et al.  Neuronal activity determines the protein synthesis dependence of long-term potentiation , 2006, Nature Neuroscience.

[7]  G. Tononi,et al.  Sleep function and synaptic homeostasis. , 2006, Sleep medicine reviews.

[8]  C. Law,et al.  Sleep-Dependent Plasticity Requires Cortical Activity , 2005, The Journal of Neuroscience.

[9]  J. Tsien,et al.  Requirement of NMDA receptor reactivation for consolidation and storage of nondeclarative taste memory revealed by inducible NR1 knockout , 2005, The European journal of neuroscience.

[10]  Michael D. Ehlers,et al.  Homeostatic plasticity and NMDA receptor trafficking , 2005, Trends in Neurosciences.

[11]  J. Born,et al.  Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[12]  G. Tononi,et al.  Local sleep and learning , 2004, Nature.

[13]  Michael Häusser,et al.  A proportional but slower NMDA potentiation follows AMPA potentiation in LTP , 2004, Nature Neuroscience.

[14]  Y. Dudai.  The neurobiology of consolidations, or, how stable is the engram? , 2004, Annual review of psychology.

[15]  M. Lavine,et al.  Long-Lasting Novelty-Induced Neuronal Reverberation during Slow-Wave Sleep in Multiple Forebrain Areas , 2004, PLoS biology.

[16]  J. Lisman.  Long-term potentiation: outstanding questions and attempted synthesis. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  B. Platt,et al.  Glutamate receptor function in learning and memory , 2003, Behavioural Brain Research.

[18]  P. Maquet,et al.  Neural correlates of perceptual learning: A functional MRI study of visual texture discrimination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Joe Z. Tsien,et al.  An emerging molecular and cellular framework for memory processing by the hippocampus , 2002, Trends in Neurosciences.

[20]  B L McNaughton,et al.  Memory reactivation and consolidation during sleep: from cellular mechanisms to human performance. , 2002, Progress in brain research.

[21]  K. Ehrenberger,et al.  Different action of memantine and caroverine on glutamatergic transmission in the mammalian cochlea. , 2002, Advances in oto-rhino-laryngology.

[22]  S. Kapur,et al.  NMDA receptor antagonists ketamine and PCP have direct effects on the dopamine D2 and serotonin 5-HT2 receptors—implications for models of schizophrenia , 2002, Molecular Psychiatry.

[23]  L. Cohen,et al.  Mechanisms underlying rapid experience-dependent plasticity in the human visual cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[24]  G. Orban,et al.  Practising orientation identification improves orientation coding in V1 neurons , 2001, Nature.

[25]  Ary S. Ramoa,et al.  Suppression of Cortical NMDA Receptor Function Prevents Development of Orientation Selectivity in the Primary Visual Cortex , 2001, The Journal of Neuroscience.

[26]  M. Stryker,et al.  Sleep Enhances Plasticity in the Developing Visual Cortex , 2001, Neuron.

[27]  M Sur,et al.  Specific Roles of NMDA and AMPA Receptors in Direction-Selective and Spatial Phase-Selective Responses in Visual Cortex , 2001, The Journal of Neuroscience.

[28]  J. Born,et al.  Early sleep triggers memory for early visual discrimination skills , 2000, Nature Neuroscience.

[29]  J. Hobson,et al.  Visual discrimination learning requires sleep after training , 2000, Nature Neuroscience.

[30]  E. Shimizu,et al.  NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. , 2000, Science.

[31]  D. Margoliash,et al.  Song replay during sleep and computational rules for sensorimotor vocal learning. , 2000, Science.

[32]  Axel Cleeremans,et al.  Experience-dependent changes in cerebral activation during human REM sleep , 2000, Nature Neuroscience.

[33]  R. Nicoll,et al.  Synaptic plasticity and dynamic modulation of the postsynaptic membrane , 2000, Nature Neuroscience.

[34]  J. Csicsvari,et al.  Replay and Time Compression of Recurring Spike Sequences in the Hippocampus , 1999, The Journal of Neuroscience.

[35]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[36]  Mark F. Bear,et al.  Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo , 1999, Nature Neuroscience.

[37]  K. Fox,et al.  Injection of MK-801 affects ocular dominance shifts more than visual activity. , 1996, Journal of neurophysiology.

[38]  Is drinking water sold in vending machines safe for people with HIV? , 1998, Positive living.

[39]  S. Rumpel,et al.  Silent Synapses in the Developing Rat Visual Cortex: Evidence for Postsynaptic Expression of Synaptic Plasticity , 1998, The Journal of Neuroscience.

[40]  G Buzsáki,et al.  Memory consolidation during sleep: a neurophysiological perspective. , 1998, Journal of sleep research.

[41]  U. Frey,et al.  Synaptic tagging and long-term potentiation , 1997, Nature.

[42]  M. Bear,et al.  This paper was presented at a colloquium entitled ‘ ‘ Memory : Recording Experience in Cells and Circuits , ’ ’ organized by , 1996 .

[43]  M. Bear,et al.  Experience-dependent modification of synaptic plasticity in visual cortex , 1996, Nature.

[44]  A. Karni,et al.  Dependence on REM sleep of overnight improvement of a perceptual skill. , 1994, Science.

[45]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[46]  N. Rickard,et al.  Both non-NMDA and NMDA glutamate receptors are necessary for memory consolidation in the day-old chick. , 1994, Behavioral and neural biology.

[47]  V. Bigl,et al.  Postnatal development of NMDA, AMPA and kainate receptors in individual layers of rat visual cortex and the effect of monocular deprivation , 1994, International Journal of Developmental Neuroscience.

[48]  A. Karni,et al.  The time course of learning a visual skill , 1993, Nature.

[49]  N W Daw,et al.  The role of NMDA receptors in information processing. , 1993, Annual review of neuroscience.

[50]  G. Carmignoto,et al.  Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. , 1992, Science.

[51]  D Sagi,et al.  Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[52]  J. Rauschecker,et al.  Effects of NMDA antagonists on developmental plasticity in kitten visual cortex , 1990, International Journal of Developmental Neuroscience.

[53]  K D Miller,et al.  Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[54]  N. Daw,et al.  The location and function of NMDA receptors in cat and kitten visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  W. Singer,et al.  Long-term potentiation and NMDA receptors in rat visual cortex , 1987, Nature.

[56]  I. Kodama,et al.  Electromechanical Effects of Caroverine, a New Slow‐Channel Blockade, on the SA Node Cells of Rabbit and Atrial Muscle Fibers of Rabbit and Guinea Pig , 1982, Journal of cardiovascular pharmacology.

[57]  C. Gilbert,et al.  Aspartate and glutamate as possible neurotransmitters of cells in layer 6 of the visual cortex , 1980, Nature.