Gamma band plasticity in sensory cortex is a signature of the strongest memory rather than memory of the training stimulus

Gamma oscillations (∼30-120Hz) are considered to be a reflection of coordinated neuronal activity, linked to processes underlying synaptic integration and plasticity. Increases in gamma power within the cerebral cortex have been found during many cognitive processes such as attention, learning, memory and problem solving in both humans and animals. However, the specificity of gamma to the detailed contents of memory remains largely unknown. We investigated the relationship between learning-induced increased gamma power in the primary auditory cortex (A1) and the strength of memory for acoustic frequency. Adult male rats (n=16) received three days (200 trials each) of pairing a tone (3.66 kHz) with stimulation of the nucleus basalis, which implanted a memory for acoustic frequency as assessed by associatively-induced disruption of ongoing behavior, viz., respiration. Post-training frequency generalization gradients (FGGs) revealed peaks at non-CS frequencies in 11/16 cases, likely reflecting normal variation in pre-training acoustic experiences. A stronger relationship was found between increased gamma power and the frequency with the strongest memory (peak of the difference between individual post- and pre-training FGGs) vs. behavioral responses to the CS training frequency. No such relationship was found for the theta/alpha band (4-15 Hz). These findings indicate that the strength of specific increased neuronal synchronization within primary sensory cortical fields can determine the specific contents of memory.

[1]  Norman M. Weinberger,et al.  Sensory memory consolidation observed: Increased specificity of detail over days , 2009, Neurobiology of Learning and Memory.

[2]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[3]  Per B. Sederberg,et al.  Oscillatory correlates of the primacy effect in episodic memory , 2006, NeuroImage.

[4]  N. Weinberger.  Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. , 2007, Learning & memory.

[5]  D. Rasmusson,et al.  Phasic relationship between the activity of basal forebrain neurons and cortical EEG in urethane-anesthetized rat , 1997, Brain Research.

[6]  Larry L. Butcher,et al.  Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: A combined fluorescent tracer and acetylcholinesterase analysis , 1982, Brain Research Bulletin.

[7]  Christoph Braun,et al.  Coherence of gamma-band EEG activity as a basis for associative learning , 1999, Nature.

[8]  Werner Lutzenberger,et al.  Dynamics of Gamma-Band Activity during an Audiospatial Working Memory Task in Humans , 2002, The Journal of Neuroscience.

[9]  P. Fries.  A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[10]  J. Isaac,et al.  Hippocampal Place Cell Firing Patterns Can Induce Long-Term Synaptic Plasticity In Vitro , 2009, The Journal of Neuroscience.

[11]  S. Grossberg,et al.  Spikes, synchrony, and attentive learning by laminar thalamocortical circuits , 2006, Brain Research.

[12]  W. Freeman,et al.  Change in pattern of ongoing cortical activity with auditory category learning , 2001, Nature.

[13]  W. Singer,et al.  Phase Sensitivity of Synaptic Modifications in Oscillating Cells of Rat Visual Cortex , 2004, The Journal of Neuroscience.

[14]  N. Weinberger,et al.  CS-specific gamma, theta, and alpha EEG activity detected in stimulus generalization following induction of behavioral memory by stimulation of the nucleus basalis , 2003, Neurobiology of Learning and Memory.

[15]  S. Epstein,et al.  Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model , 2008, Proceedings of the National Academy of Sciences.

[16]  E. Rolls,et al.  Neuronal responses related to reinforcement in the primate basal forebrain , 1990, Brain Research.

[17]  G L Gerstein,et al.  Daily variation and appetitive conditioning‐induced plasticity of auditory cortex receptive fields , 2001, The European journal of neuroscience.

[18]  H H Jasper,et al.  Acetylcholine Liberation from Cerebral Cortex during Paradoxical (REM) Sleep , 1971, Science.

[19]  Norman M Weinberger,et al.  The nucleus basalis and memory codes: Auditory cortical plasticity and the induction of specific, associative behavioral memory , 2003, Neurobiology of Learning and Memory.

[20]  C. L. Cox,et al.  Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  Norman M. Weinberger,et al.  Learning strategy trumps motivational level in determining learning-induced auditory cortical plasticity , 2010, Neurobiology of Learning and Memory.

[22]  M. Dimyan,et al.  Induction of long-term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. , 1998, Behavioral neuroscience.

[23]  David I. Mostofsky,et al.  Stimulus generalization : the papers presented at the Conference on Stimulus Generalization held at Boston Univ., June, 1963 , 1965 .

[24]  J. Fell,et al.  The role of phase synchronization in memory processes , 2011, Nature Reviews Neuroscience.

[25]  N Suga,et al.  Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  N. Weinberger,et al.  Consolidation and long-term retention of an implanted behavioral memory , 2011, Neurobiology of Learning and Memory.

[27]  J. Bakin,et al.  Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[28]  T. Sejnowski,et al.  Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models , 2000, The Journal of Neuroscience.

[29]  D. Rasmusson,et al.  The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex , 1999, Progress in Neurobiology.

[30]  M. Kilgard,et al.  Cortical map reorganization enabled by nucleus basalis activity. , 1998, Science.

[31]  Andreas Keil,et al.  Modulation of induced gamma band responses and phase synchrony in a paired associate learning task in the human EEG , 2001, Neuroscience Letters.

[32]  L. Bianchi,et al.  Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats , 2001, Neuroscience.

[33]  E G Cape,et al.  Effects of glutamate agonist versus procaine microinjections into the basal forebrain cholinergic cell area upon gamma and theta EEG activity and sleep–wake state , 2000, The European journal of neuroscience.

[34]  N. Weinberger,et al.  Induction of behavioral associative memory by stimulation of the nucleus basalis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  N. Weinberger,et al.  Specific auditory memory induced by nucleus basalis stimulation depends on intrinsic acetylcholine , 2008, Neurobiology of Learning and Memory.

[36]  R. Oostenveld,et al.  Theta and Gamma Oscillations Predict Encoding and Retrieval of Declarative Memory , 2006, The Journal of Neuroscience.

[37]  N. Weinberger,et al.  Motivationally neutral stimulation of the nucleus basalis induces specific behavioral memory , 2008, Neurobiology of Learning and Memory.

[38]  R. B. Purtle.  Peak shift: A review. , 1973 .

[39]  K. Spence.  The differential response in animals to stimuli varying within a single dimension. , 1937 .

[40]  Roger D. Traub,et al.  Dual Gamma Rhythm Generators Control Interlaminar Synchrony in Auditory Cortex , 2011, The Journal of Neuroscience.

[41]  J. Knott.  The organization of behavior: A neuropsychological theory , 1951 .

[42]  Norman M. Weinberger,et al.  Remodeling the cortex in memory: Increased use of a learning strategy increases the representational area of relevant acoustic cues , 2010, Neurobiology of Learning and Memory.

[43]  Adriano B. L. Tort,et al.  Theta–gamma coupling increases during the learning of item–context associations , 2009, Proceedings of the National Academy of Sciences.

[44]  D. C. Mccarthy,et al.  Hippocampal and neocortical gamma oscillations predict memory formation in humans. , 2006, Cerebral cortex.

[45]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[46]  N. Suga,et al.  Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. , 2003, Journal of neurophysiology.

[47]  Michael M Merzenich,et al.  Perceptual Learning Directs Auditory Cortical Map Reorganization through Top-Down Influences , 2006, The Journal of Neuroscience.

[48]  J. Edeline,et al.  Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. , 1993, Behavioral neuroscience.

[49]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[50]  T. Hattori,et al.  Separate neuronal populations of the rat globus pallidus projecting to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental area , 1992, Neuroscience.

[51]  M. Berger,et al.  High gamma activity in response to deviant auditory stimuli recorded directly from human cortex. , 2005, Journal of neurophysiology.

[52]  Norman M. Weinberger,et al.  Detection of an inhibitory cortical gradient underlying peak shift in learning: A neural basis for a false memory , 2012, Neurobiology of Learning and Memory.

[53]  N. Weinberger.  The medial geniculate, not the amygdala, as the root of auditory fear conditioning , 2011, Hearing Research.

[54]  N. Weinberger,et al.  Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity , 2001, Neuroreport.

[55]  Gastone G. Celesia,et al.  Acetylcholine released from cerebral cortex in relation to state of activation , 1966, Neurology.

[56]  N. Weinberger,et al.  The effects of electrical stimulation of the nucleus basalis on the electroencephalogram, heart rate, and respiration. , 2002, Behavioral neuroscience.

[57]  W. Singer,et al.  Short- and Long-Term Effects of Cholinergic Modulation on Gamma Oscillations and Response Synchronization in the Visual Cortex , 2004, The Journal of Neuroscience.

[58]  A. Duque,et al.  EEG correlation of the discharge properties of identified neurons in the basal forebrain. , 2000, Journal of neurophysiology.

[59]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[60]  A. Thiele,et al.  Cholinergic modulation of response properties and orientation tuning of neurons in primary visual cortex of anaesthetized Marmoset monkeys , 2006, The European journal of neuroscience.

[61]  M. Dimyan,et al.  Basal forebrain stimulation induces discriminative receptive field plasticity in the auditory cortex. , 1999, Behavioral neuroscience.

[62]  Norman M. Weinberger,et al.  Rapid induction of specific associative behavioral memory by stimulation of the nucleus basalis in the rat , 2006, Neurobiology of Learning and Memory.

[63]  L. M. Ward,et al.  Theta modulation of inter-regional gamma synchronization during auditory attention control , 2012, Brain Research.

[64]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[65]  Norman M. Weinberger,et al.  Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig , 1990, Brain Research.

[66]  Norman M Weinberger,et al.  Extinction reveals that primary sensory cortex predicts reinforcement outcome , 2012, The European journal of neuroscience.

[67]  Drew B Headley,et al.  Gamma-Band Activation Predicts Both Associative Memory and Cortical Plasticity , 2011, The Journal of Neuroscience.

[68]  W. Singer,et al.  Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential , 1998, Neuroscience.

[69]  N. Weinberger.  Specific long-term memory traces in primary auditory cortex , 2004, Nature Reviews Neuroscience.

[70]  M. Andrés.  Learning and behavior: A contemporary synthesis , 2008 .

[71]  Norman M. Weinberger,et al.  The level of cholinergic nucleus basalis activation controls the specificity of auditory associative memory , 2006, Neurobiology of Learning and Memory.

[72]  G. Lynch,et al.  The neurobiology of learning and memory , 1989, Cognition.