This Reprint May Differ from the Original in Pagination and Typographic Detail. Disrupting Neural Activity Related to Awake-state Sharp Wave-ripple Complexes Prevents Hippocampal Learning Disrupting Neural Activity Related to Awake-state Sharp Wave-ripple Complexes Prevents Hippocampal Learning

Oscillations in hippocampal local-field potentials (LFPs) reflect the crucial involvement of the hippocampus in memory trace formation: theta (4–8 Hz) oscillations and ripples (~200 Hz) occurring during sharp waves are thought to mediate encoding and consolidation, respectively. During sharp wave-ripple complexes (SPW-Rs), hippocampal cell firing closely follows the pattern that took place during the initial experience, most likely reflecting replay of that event. Disrupting hippocampal ripples using electrical stimulation either during training in awake animals or during sleep after training retards spatial learning. Here, adult rabbits were trained in trace eyeblink conditioning, a hippocampus-dependent associative learning task. A bright light was presented to the animals during the inter-trial interval (ITI), when awake, either during SPW-Rs or irrespective of their neural state. Learning was particularly poor when the light was presented following SPW-Rs. While the light did not disrupt the ripple itself, it elicited a theta-band oscillation, a state that does not usually coincide with SPW-Rs. Thus, it seems that consolidation depends on neuronal activity within and beyond the hippocampus taking place immediately after, but by no means limited to, hippocampal SPW-Rs.

[1]  L. Frank,et al.  Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory , 2012, Science.

[2]  J J Kim,et al.  Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. , 1995, Behavioral neuroscience.

[3]  Sean M Montgomery,et al.  Theta and Gamma Coordination of Hippocampal Networks during Waking and Rapid Eye Movement Sleep , 2008, The Journal of Neuroscience.

[4]  M. Hasselmo,et al.  The hippocampus as an associator of discontiguous events , 1998, Trends in Neurosciences.

[5]  H. Eichenbaum,et al.  Hippocampal “Time Cells” Bridge the Gap in Memory for Discontiguous Events , 2011, Neuron.

[6]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[7]  Matthijs A. A. van der Meer,et al.  Hippocampal Replay Is Not a Simple Function of Experience , 2010, Neuron.

[8]  Jan Born,et al.  Slow oscillations orchestrating fast oscillations and memory consolidation. , 2011, Progress in brain research.

[9]  I. Gormezano,et al.  Acquisition and Extinction of the Classically Conditioned Eyelid Response in the Albino Rabbit , 1962, Science.

[10]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[11]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

[12]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[13]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[14]  Mattias P. Karlsson,et al.  Awake replay of remote experiences in the hippocampus , 2009, Nature Neuroscience.

[15]  Matthew A. Wilson,et al.  Hippocampal Replay of Extended Experience , 2009, Neuron.

[16]  Sean M Montgomery,et al.  Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm , 2008, Neuron.

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

[18]  J. Born,et al.  The memory function of sleep , 2010, Nature Reviews Neuroscience.

[19]  G. Buzsáki Hippocampal sharp waves: Their origin and significance , 1986, Brain Research.

[20]  L. Squire Memory systems of the brain: A brief history and current perspective , 2004, Neurobiology of Learning and Memory.

[21]  J. O’Neill,et al.  Play it again: reactivation of waking experience and memory , 2010, Trends in Neurosciences.

[22]  Yutaka Kirino,et al.  Time-Dependent Reorganization of the Brain Components Underlying Memory Retention in Trace Eyeblink Conditioning , 2003, The Journal of Neuroscience.

[23]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[24]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[25]  J. Disterhoft,et al.  Sequence of single neuron changes in CA1 hippocampus of rabbits during acquisition of trace eyeblink conditioned responses. , 1997, Journal of neurophysiology.

[26]  J. Bureš,et al.  Electrophysiological methods in biological research , 1960 .

[27]  V. Bracha,et al.  A long-range, wide field-of-view infrared eyeblink detector , 2006, Journal of Neuroscience Methods.

[28]  H. Tanila,et al.  Artificial Theta Stimulation Impairs Encoding of Contextual Fear Memory , 2012, PloS one.

[29]  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.

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

[31]  M. Penttonen,et al.  Hippocampo–cerebellar theta band phase synchrony in rabbits , 2010, Neuroscience.

[32]  J. Palva,et al.  Phase Synchrony among Neuronal Oscillations in the Human Cortex , 2005, The Journal of Neuroscience.

[33]  Markku Penttonen,et al.  Hippocampal Ripple-Contingent Training Accelerates Trace Eyeblink Conditioning and Retards Extinction in Rabbits , 2010, The Journal of Neuroscience.