Paradoxical sleep: A vigilance state to gate long-term brain plasticity?

Memory consolidation is the process for long-term storage of information and protection against interferences. It has been proposed that long-term potentiation (LTP), the long-lasting enhancement of synaptic transmission, is a cellular model for memory consolidation. Since consolidation of several forms of memory is facilitated by paradoxical sleep (PS) we ask whether PS modulates the cellular and molecular pathways underlying LTP. The long-lasting form of LTP (L-LTP) is dependent on the activation of transcription factors, enzymatic cascades and the secreted neurotrophin BDNF. By using PS deprivation, immunohistochemistry and quantitative real-time polymerase chain reaction (qPCR), we showed that an increase in PS amount (produced by rebound in PS deprived rats) is able to up-regulate the expression level of transcription factors Zif268 and c-Fos as well as Arc and BDNF in the CA1 and CA3 areas of the hippocampus. Several studies involved these factors in dendritic protein synthesis and in long-term structural changes of synapses underlying L-LTP. The present study together with the work of others (Ribeiro et al., 2002) suggest that by this mechanism, a post-learning increase in PS quantity (post-learning PS window) could convert a transient form of LTP to L-LTP.

[1]  J. Winson,et al.  Gating of neuronal transmission in the hippocampus: efficacy of transmission varies with behavioral state. , 1977, Science.

[2]  Carlyle Smith,et al.  Sleep states, memory processes and synaptic plasticity , 1996, Behavioural Brain Research.

[3]  R. Morris,et al.  Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. , 2010, Annual review of psychology.

[4]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[5]  Jeffrey C Magee,et al.  Sleep Deprivation Causes Behavioral, Synaptic, and Membrane Excitability Alterations in Hippocampal Neurons , 2003, The Journal of Neuroscience.

[6]  B. Hars,et al.  Processing of learned information in paradoxical sleep: relevance for memory , 1995, Behavioural Brain Research.

[7]  W. Gan,et al.  Sleep promotes branch-specific formation of dendritic spines after learning , 2014, Science.

[8]  S. Davis,et al.  The transcription factor Zif268/Egr1, brain plasticity, and memory. , 2014, Progress in molecular biology and translational science.

[9]  R J Wyatt,et al.  The flower pot technique of rapid eye movement (REM) sleep deprivation. , 1974, Pharmacology, biochemistry, and behavior.

[10]  W. Dement,et al.  Cyclic variations in EEG during sleep and their relation to eye movements, body motility, and dreaming. , 1957, Electroencephalography and clinical neurophysiology.

[11]  R. Anwyl,et al.  Stimulation on the Positive Phase of Hippocampal Theta Rhythm Induces Long-Term Potentiation That Can Be Depotentiated by Stimulation on the Negative Phase in Area CA1 In Vivo , 1997, The Journal of Neuroscience.

[12]  C. Bramham,et al.  BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis , 2005, Progress in Neurobiology.

[13]  G. Tononi,et al.  Extensive and Divergent Effects of Sleep and Wakefulness on Brain Gene Expression , 2004, Neuron.

[14]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

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

[16]  P. Frankland,et al.  The organization of recent and remote memories , 2005, Nature Reviews Neuroscience.

[17]  Francesco Marrosu,et al.  Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats , 1995, Brain Research.

[18]  M. Hasselmo.  The role of acetylcholine in learning and memory , 2006, Current Opinion in Neurobiology.

[19]  S. Tonegawa,et al.  A clustered plasticity model of long-term memory engrams , 2006, Nature Reviews Neuroscience.

[20]  M. Walker,et al.  Sleep, Plasticity and Memory from Molecules to Whole-Brain Networks , 2013, Current Biology.

[21]  G. Tononi,et al.  Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration , 2014, Neuron.

[22]  Carlyle T. Smith,et al.  Sleep states and memory processes , 1995, Behavioural Brain Research.

[23]  Jean-Christophe Comte,et al.  Paradoxical (REM) sleep deprivation causes a large and rapidly reversible decrease in long-term potentiation, synaptic transmission, glutamate receptor protein levels, and ERK/MAPK activation in the dorsal hippocampus. , 2009, Sleep.

[24]  R. Buckner,et al.  REM Sleep, Prefrontal Theta, and the Consolidation of Human Emotional Memory , 2008, Cerebral cortex.

[25]  G. Tononi,et al.  Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep , 2008, Nature Neuroscience.

[26]  C. Bramham,et al.  Synaptic plasticity in the hippocampus is modulated by behavioral state , 1989, Brain Research.

[27]  Nelson A. M. Lemos,et al.  Novel Experience Induces Persistent Sleep-Dependent Plasticity in the Cortex but not in the Hippocampus , 2007, Front. Neurosci..

[28]  S. Ribeiro,et al.  Induction of Hippocampal Long-Term Potentiation during Waking Leads to Increased Extrahippocampal zif-268 Expression during Ensuing Rapid-Eye-Movement Sleep , 2002, The Journal of Neuroscience.

[29]  P Maquet,et al.  The Role of Sleep in Learning and Memory , 2001, Science.

[30]  C. Degueldre,et al.  Functional neuroanatomy of human rapid-eye-movement sleep and dreaming , 1996, Nature.

[31]  E. Wagner,et al.  Impaired Long-Term Memory and NR2A-Type NMDA Receptor-Dependent Synaptic Plasticity in Mice Lacking c-Fos in the CNS , 2003, The Journal of Neuroscience.

[32]  J. Born,et al.  About sleep's role in memory. , 2013, Physiological reviews.

[33]  P. Worley,et al.  The Immediate Early Gene Arc/Arg3.1: Regulation, Mechanisms, and Function , 2008, The Journal of Neuroscience.

[34]  Jonathan R. Whitlock,et al.  Learning Induces Long-Term Potentiation in the Hippocampus , 2006, Science.

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

[36]  M. Walker.  The Role of Sleep in Cognition and Emotion , 2009, Annals of the New York Academy of Sciences.

[37]  S. Ribeiro,et al.  Brain gene expression during REM sleep depends on prior waking experience. , 1999, Learning & memory.

[38]  C. Pavlides,et al.  Lonf-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity , 1988, Brain Research.

[39]  G. Buzsáki,et al.  REM Sleep Reorganizes Hippocampal Excitability , 2012, Neuron.

[40]  S. Datta,et al.  Activation of Phasic Pontine-Wave Generator Prevents Rapid Eye Movement Sleep Deprivation-Induced Learning Impairment in the Rat: A Mechanism for Sleep-Dependent Plasticity , 2004, The Journal of Neuroscience.

[41]  T. Bliss,et al.  A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories , 2001, Nature Neuroscience.

[42]  G. Tononi,et al.  Differential Expression of Plasticity-Related Genes in Waking and Sleep and Their Regulation by the Noradrenergic System , 2000, The Journal of Neuroscience.

[43]  Sara J. Aton,et al.  Protein Synthesis during Sleep Consolidates Cortical Plasticity In Vivo , 2012, Current Biology.