Long-Term Consolidation and Retention of Learning-Induced Tuning Plasticity in the Auditory Cortex of the Guinea Pig

The major goal of this study was to determine whether classical conditioning produces long-term neural consolidation of frequency tuning plasticity in the auditory cortex. Local field potentials (LFPs) were obtained from chronically implanted adult male Hartley guinea pigs that were divided into conditioning (n = 4) and sensitization control (n = 3) groups. Tuning functions were determined in awake subjects for average LFPs (approximately 0.4 to 36.0 kHz, -20 to 80 dB) immediately before training as well as 1 h and 1, 3, 7, and 10 days after training; sensitization subjects did not have a 10-day retention test. Conditioning consisted of a single session of 30 to 45 trials of a 6-s tone (CS, 70 dB) that was not the best frequency (BF, peak of a tuning curve), followed by a brief leg shock (US) at CS offset. Sensitization control animals received the same density of CS and US presentations unpaired. Heart rate recordings showed that the conditioning group developed conditioned bradycardia, whereas the sensitization control group did not. Local field potentials in the conditioning group, but not in the sensitization group, developed tuning plasticity. The ratio of responses to the CS frequency versus the BF were increased 1 h after training, and this increase was retained for the 10-day period of the study. Both tuning plasticity and retention were observed across stimulus levels (10-80 dB). Most noteworthy, tuning plasticity exhibited consolidation (i.e., developed greater CS-specific effects across retention periods), attaining asymptote at 3 days. The findings indicate that LFPs in the auditory cortex have three cardinal features of behavioral memory: associative tuning plasticity, long-term retention, and long-term consolidation. Potential cellular and subcellular mechanisms of LFP tuning plasticity and long-term consolidation are discussed.

[1]  Alexander A. Borbe´ly.  Changes in click-evoked responses as a function of depth in auditory cortex of the rat. , 1970, Brain research.

[2]  L. Squire,et al.  The primate hippocampal formation: evidence for a time-limited role in memory storage. , 1990, Science.

[3]  E. Schuman,et al.  A Requirement for Local Protein Synthesis in Neurotrophin-Induced Hippocampal Synaptic Plasticity , 1996, Science.

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

[5]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

[6]  E. Kandel,et al.  Genetic Demonstration of a Role for PKA in the Late Phase of LTP and in Hippocampus-Based Long-Term Memory , 1997, Cell.

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

[8]  Norman M. Weinberger,et al.  Memory codes: New concept for old problem. , 2001 .

[9]  M. Kossut,et al.  Short-lasting classical conditioning induces reversible changes of representational maps of vibrissae in mouse SI cortex--a 2DG study. , 1996, Cerebral cortex.

[10]  T. Crow,et al.  Protein synthesis-dependent and mRNA synthesis-independent intermediate phase of memory in Hermissenda. , 1999, Journal of neurophysiology.

[11]  Mary Chen,et al.  Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change , 1995, Cell.

[12]  J. D. McGaugh.  Memory--a century of consolidation. , 2000, Science.

[13]  J. Wolpaw.  Single unit activity vs. amplitude of the epidural evoked potential in primary auditory cortex of awake cats. , 1979, Electroencephalography and clinical neurophysiology.

[14]  G. V. Simpson,et al.  Cellular generators of the cortical auditory evoked potential initial component. , 1992, Electroencephalography and clinical neurophysiology.

[15]  E. Kandel,et al.  Requirement of a critical period of transcription for induction of a late phase of LTP. , 1994, Science.

[16]  T. Carew,et al.  Dynamics of Induction and Expression of Long-Term Synaptic Facilitation in Aplysia , 1996, The Journal of Neuroscience.

[17]  A. Borbély,et al.  Effects of pentobarbitone and chlorpromazine on acoustically evoked potentials in the rat. , 1970, Neuropharmacology.

[18]  N. Kraus,et al.  Subcortical and cortical components of the MLR generating system , 1991, Brain Research.

[19]  N. Weinberger,et al.  Frequency-specific receptive field plasticity in the medial geniculate body induced by pavlovian fear conditioning is expressed in the anesthetized brain. , 1992, Behavioral neuroscience.

[20]  M. Meunier,et al.  Time-dependent sequential increases in [14C]2-deoxyglucose uptake in subcortical and cortical structures during memory consolidation of an operant training in mice. , 1991, Behavioral and neural biology.

[21]  J J Eggermont,et al.  Synchrony between single-unit activity and local field potentials in relation to periodicity coding in primary auditory cortex. , 1995, Journal of neurophysiology.

[22]  O D Creutzfeldt,et al.  Functional subdivisions in the auditory cortex of the guinea pig , 1989, The Journal of comparative neurology.

[23]  J. Edeline,et al.  Thalamic short-term plasticity in the auditory system: associative returning of receptive fields in the ventral medial geniculate body. , 1991, Behavioral neuroscience.

[24]  Eric R Kandel,et al.  A novel intermediate stage in the transition between short- and long-term facilitation in the sensory to motor neuron synapse of aplysia , 1995, Neuron.

[25]  Bernice W. Polemis.  Nonparametric Statistics for the Behavioral Sciences , 1959 .

[26]  N. Mackintosh.  The psychology of animal learning , 1974 .

[27]  M. Gabriel,et al.  Changes of Cingulothalamic Topographic Excitation Patterns and Avoidance Response Incubation over Time Following Initial Discriminative Conditioning in Rabbits , 1999, Neurobiology of Learning and Memory.

[28]  M. Merzenich,et al.  Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  R. Rescorla.  Behavioral studies of Pavlovian conditioning. , 1988, Annual review of neuroscience.

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

[31]  N. Weinberger,et al.  Analysis of response systems in Pavlovian conditioning reveals rapidly versus slowly acquired conditioned responses: Support for two factors, implications for behavior and neurobiology , 1992, Psychobiology.

[32]  Lindsay Aitkin,et al.  The auditory cortex : structural and functional bases of auditory perception , 1990 .

[33]  C. Destrade,et al.  Differential learning‐stage dependent patterns of c‐Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice , 2000, The European journal of neuroscience.

[34]  R. Knight,et al.  Auditory evoked potentials from the primary auditory cortex of the cat: topographic and pharmacological studies. , 1990, Electroencephalography and clinical neurophysiology.

[35]  L. Kamin,et al.  The retention of an incompletely learned avoidance response. , 1957, Journal of comparative and physiological psychology.

[36]  D. Lindsley,et al.  Behavioral and Electroencephalographic Arousal to Contrasting Novel Stimulation , 1964, Science.

[37]  W. Lifschitz,et al.  Studies on the auditory cortex of rabbit. , 1971, Experimental neurology.

[38]  T. Préat,et al.  Genetic dissection of consolidated memory in Drosophila , 1994, Cell.

[39]  Michael A Sutton,et al.  Parallel Molecular Pathways Mediate Expression of Distinct Forms of Intermediate-Term Facilitation at Tail Sensory–Motor Synapses in Aplysia , 2000, Neuron.

[40]  T. Bullock,et al.  Signals and signs in the nervous system: the dynamic anatomy of electrical activity is probably information-rich. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Norman M. Weinberger,et al.  Long-Term Frequency Tuning of Local Field Potentials in the Auditory Cortex of the Waking Guinea Pig , 2001, Journal of the Association for Research in Otolaryngology.

[42]  A. Tunturi.  AUDIO FREQUENCY LOCALIZATION IN THE ACOUSTIC CORTEX OF THE DOG , 1944 .

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

[44]  C Bucherelli,et al.  Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat , 1999, The Journal of Neuroscience.

[45]  D. Diamond,et al.  Physiological plasticity in auditory cortex: Rapid induction by learning , 1987, Progress in Neurobiology.

[46]  U. Mitzdorf.  Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[47]  N. Suga,et al.  Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. , 1982, Journal of neurophysiology.

[48]  J. Edeline,et al.  Rapid development of learning-induced receptive field plasticity in the auditory cortex. , 1993, Behavioral neuroscience.

[49]  Norman M. Weinberger,et al.  Physiological Memory in Primary Auditory Cortex: Characteristics and Mechanisms , 1998, Neurobiology of Learning and Memory.

[50]  B. Bontempi,et al.  Time-dependent reorganization of brain circuitry underlying long-term memory storage , 1999, Nature.

[51]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[52]  D. Barth,et al.  Three-dimensional analysis of auditory-evoked potentials in rat neocortex. , 1990, Journal of neurophysiology.

[53]  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.

[54]  D R Humphrey,et al.  Re-analysis of the antidromic cortical response. II. On the contribution of cell discharge and PSPs to the evoked potentials. , 1968, Electroencephalography and clinical neurophysiology.

[55]  O D Creutzfeldt,et al.  Relations between EEG phenomena and potentials of single cortical cells. II. Spontaneous and convulsoid activity. , 1966, Electroencephalography and clinical neurophysiology.

[56]  Walloch Ra.  Cortical evoked potentials recorded from the guinea pig without averaging. , 1975 .

[57]  E. N. Sokolov,et al.  Perception and the Conditioned Reflex , 1965 .

[58]  Norman M. Weinberger,et al.  Induction of receptive field plasticity in the auditory cortex of the guinea pig during instrumental avoidance conditioning. , 1996 .

[59]  G. Karmos,et al.  Intracortical auditory evoked potentials during classical aversive conditioning in cats , 1988, Biological Psychology.

[60]  N. Weinberger.  Dynamic regulation of receptive fields and maps in the adult sensory cortex. , 1995, Annual Review of Neuroscience.

[61]  Donald Robertson,et al.  Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness , 1989, The Journal of comparative neurology.

[62]  U. Frey,et al.  Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro , 1988, Brain Research.

[63]  R. Galamboš,et al.  Electrophysiological correlates of a conditioned response in cats. , 1956, Science.

[64]  N. Weinberger,et al.  Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[65]  R A Walloch.  Cortical evoked potentials recorded from the guinea pig without averaging. , 1975, Acta oto-laryngologica.

[66]  B. Bontempi,et al.  Differential Temporal Evolution of Post‐Training Changes in Regional Brain Glucose Metabolism Induced by Repeated Spatial Discrimination Training in Mice: Visualization of the Memory Consolidation Process? , 1996, The European journal of neuroscience.

[67]  R. Pujol,et al.  A laminar study of evoked potentials and unit responses in the auditory cortex of the postnatal cat. , 1972, Brain research.

[68]  D. Diamond,et al.  Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. , 1989, Behavioral neuroscience.

[69]  K. Kaga,et al.  Evidence for a primary cortical origin of a middle latency auditory evoked potential in cats. , 1980, Electroencephalography and clinical neurophysiology.

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

[71]  W. Quinn,et al.  Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila , 1994, Cell.