Enhancement of Neocortical-Medial Temporal EEG Correlations during Non-REM Sleep

Interregional interactions of oscillatory activity are crucial for the integrated processing of multiple brain regions. However, while the EEG in virtually all brain structures passes through substantial modifications during sleep, it is still an open question whether interactions between neocortical and medial temporal EEG oscillations also depend on the state of alertness. Several previous studies in animals and humans suggest that hippocampal-neocortical interactions crucially depend on the state of alertness (i.e., waking state or sleep). Here, we analyzed scalp and intracranial EEG recordings during sleep and waking state in epilepsy patients undergoing presurgical evaluation. We found that the amplitudes of oscillations within the medial temporal lobe and the neocortex were more closely correlated during sleep, in particular during non-REM sleep, than during waking state. Possibly, the encoding of novel sensory inputs, which mainly occurs during waking state, requires that medial temporal dynamics are rather independent from neocortical dynamics, while the consolidation of memories during sleep may demand closer interactions between MTL and neocortex.

[1]  A. Rechtschaffen A manual of Standardized Terminology , 1968 .

[2]  E. Wolpert A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[3]  Miss A.O. Penney (b) , 1974, The New Yale Book of Quotations.

[4]  J. Siegel,et al.  Sleep , 2007, Neuromolecular medicine.

[5]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[6]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[7]  D. Amaral,et al.  Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex , 1991, The Journal of comparative neurology.

[8]  L. Squire,et al.  Neuroanatomy of memory. , 1993, Annual review of neuroscience.

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

[10]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

[11]  P. Nunez,et al.  Spatial filtering and neocortical dynamics: estimates of EEG coherence , 1998, IEEE Transactions on Biomedical Engineering.

[12]  C. Elger,et al.  Depth electrode implantation in the length axis of the hippocampus for the presurgical evaluation of medial temporal lobe epilepsy: a computed tomography-based stereotactic insertion technique and its accuracy. , 1998, Neurosurgery.

[13]  M. Hasselmo Neuromodulation: acetylcholine and memory consolidation , 1999, Trends in Cognitive Sciences.

[14]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[15]  E. Halgren,et al.  Early widespread cortical distribution of coherent fusiform face selective activity , 2000, Human brain mapping.

[16]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[17]  M. Wilson,et al.  Temporally Structured Replay of Awake Hippocampal Ensemble Activity during Rapid Eye Movement Sleep , 2001, Neuron.

[18]  R. Stickgold,et al.  Sleep, Learning, and Dreams: Off-line Memory Reprocessing , 2001, Science.

[19]  Kevin Barraclough,et al.  I and i , 2001, BMJ : British Medical Journal.

[20]  K. Linkenkaer-Hansen,et al.  Interhemispheric phase synchrony and amplitude correlation of spontaneous beta oscillations in human subjects: a magnetoencephalographic study , 2001, Neuroreport.

[21]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[22]  M. Steriade Neuronal Substrates of Sleep and Epilepsy , 2003 .

[23]  Marc W Howard,et al.  Theta and Gamma Oscillations during Encoding Predict Subsequent Recall , 2003, The Journal of Neuroscience.

[24]  J. Fell,et al.  Rhinal–hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization? , 2003, The European journal of neuroscience.

[25]  R. Stickgold,et al.  Sleep-Dependent θ Oscillations in the Human Hippocampus and Neocortex , 2003, The Journal of Neuroscience.

[26]  J. Csicsvari,et al.  Communication between neocortex and hippocampus during sleep in rodents , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  G. Buzsáki,et al.  Place Representation within Hippocampal Networks Is Modified by Long-Term Potentiation , 2003, Neuron.

[28]  J. Born,et al.  Declarative memory consolidation: mechanisms acting during human sleep. , 2004, Learning & memory.

[29]  Alcino J. Silva,et al.  New Circuits for Old Memories The Role of the Neocortex in Consolidation , 2004, Neuron.

[30]  Robert Stickgold,et al.  Gamma EEG dynamics in neocortex and hippocampus during human wakefulness and sleep , 2004, NeuroImage.

[31]  M. D’Esposito,et al.  Category-specific modulation of inferior temporal activity during working memory encoding and maintenance. , 2004, Brain research. Cognitive brain research.

[32]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[33]  R. Stickgold Sleep-dependent memory consolidation , 2005, Nature.

[34]  J. Fell,et al.  Memory formation by neuronal synchronization , 2006, Brain Research Reviews.

[35]  N. Kanwisher,et al.  Domain specificity in visual cortex. , 2006, Cerebral cortex.

[36]  J. Born,et al.  Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. , 2006, Journal of neurophysiology.

[37]  Sean M Montgomery,et al.  Integration and Segregation of Activity in Entorhinal-Hippocampal Subregions by Neocortical Slow Oscillations , 2006, Neuron.

[38]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[39]  J. Born,et al.  Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. , 2007, Brain : a journal of neurology.

[40]  István Ulbert,et al.  Specific increase of human entorhinal population synaptic and neuronal activity during retrieval , 2007, NeuroImage.

[41]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[42]  B. Nolan Boosting slow oscillations during sleep potentiates memory , 2008 .

[43]  Aaas News,et al.  Book Reviews , 1893, Buffalo Medical and Surgical Journal.