Theta-contingent Trial Presentation Accelerates Learning Rate and Enhances Hippocampal Plasticity during Trace Eyeblink Conditioning

Hippocampal theta activity has been established as a key predictor of acquisition rate in rabbit (Orcytolagus cuniculus) classical conditioning. The current study used an online brain--computer interface to administer conditioning trials only in the explicit presence or absence of spontaneous theta activity in the hippocampus-dependent task of trace conditioning. The findings indicate that animals given theta-contingent training learned significantly faster than those given nontheta-contingent training. In parallel with the behavioral results, the theta-triggered group, and not the nontheta-triggered group, exhibited profound increases in hippocampal conditioned unit responses early in training. The results not only suggest that theta-contingent training has a dramatic facilitory effect on trace conditioning but also implicate theta activity in enhancing the plasticity of hippocampal neurons.

[1]  J. D. Green,et al.  Hippocampal electrical activity in arousal. , 1954, Journal of neurophysiology.

[2]  W. R. Adey.  Neurophysiological correlates of information transaction and storage in brain tissue , 1965 .

[3]  J. B. Sidowski,et al.  Experimental methods and instrumentation in psychology , 1966 .

[4]  J. Sprague,et al.  Progress in physiological psychology , 1966 .

[5]  Vanderwolf Ch.  Limbic-diencephalic mechanisms of voluntary movement. , 1971 .

[6]  J. Theios,et al.  Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). , 1972, Journal of comparative and physiological psychology.

[7]  W. F. Prokasy,et al.  Classical conditioning II: Current research and theory. , 1972 .

[8]  P. Solomon,et al.  Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation. , 1975, Journal of comparative and physiological psychology.

[9]  T. L. Bennett.  The Electrical Activity of the Hippocampus and Processes of Attention , 1975 .

[10]  Richard F. Thompson,et al.  Neuronal plasticity in the limbic system during classical conditioning of the rabbit nictitating membrane response. I. The hippocampus , 1978, Brain Research.

[11]  Richard F. Thompson,et al.  Neuronal plasticity in the limbic system during classical conditioning of the rabbit nictitating membrane response. II: Septum and mammillary bodies , 1978, Brain Research.

[12]  S. D. Berry,et al.  Prediction of learning rate from the hippocampal electroencephalogram. , 1978, Science.

[13]  J. Winson.  Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. , 1978, Science.

[14]  S. D. Berry,et al.  Medial septal lesions retard classical conditioning of the nicitating membrane response in rabbits. , 1979, Science.

[15]  F. H. Lopes da Silva,et al.  The spectral properties of hippocampal EEG related to behaviour in man. , 1980, Electroencephalography and clinical neurophysiology.

[16]  M. Girgis,et al.  A new stereotaxic atlas of the rabbit brain , 1981 .

[17]  R. F. Thompson,et al.  Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. , 1983, Journal of neurophysiology.

[18]  G. A. Clark,et al.  Effects of lesions of cerebellar nuclei on conditioned behavioral and hippocampal neuronal responses , 1984, Brain Research.

[19]  G. Lynch,et al.  Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation , 1986, Brain Research.

[20]  R. F. Thompson,et al.  Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. , 1986, Behavioral neuroscience.

[21]  Richard F. Thompson,et al.  Classical conditioning, 3rd ed. , 1987 .

[22]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm , 1988, Brain Research.

[23]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. , 1988, Brain research.

[24]  S. D. Berry,et al.  Water deprivation optimizes hippocampal activity and facilitates nictitating membrane conditioning. , 1989, Behavioral neuroscience.

[25]  D. Alkon,et al.  Hippocampal lesions impair memory of short-delay conditioned eye blink in rabbits. , 1989, Behavioral neuroscience.

[26]  Scopolamine disruption of septo-hippocampal activity and classical conditioning. , 1989, Behavioral neuroscience.

[27]  D. Olton,et al.  Cholinergic and GABAergic modulation of medial septal area: effect on working memory. , 1990, Behavioral neuroscience.

[28]  J. Disterhoft,et al.  Hippocampectomy disrupts trace eye-blink conditioning in rabbits. , 1990, Behavioral neuroscience.

[29]  B. L. McNaughton,et al.  Reversible inactivation of the medial septum differentially affects two forms of learning in rats , 1990, Brain Research.

[30]  G. Lynch,et al.  A test of the spine resistance hypothesis for LTP expression , 1991, Brain Research.

[31]  A M Murro,et al.  Behavioral state‐specific changes in human hippocampal theta activity , 1991, Neurology.

[32]  H. Eichenbaum,et al.  The hippocampus--what does it do? , 1992, Behavioral and neural biology.

[33]  N. Schmajuk,et al.  Stimulus configuration, classical conditioning, and hippocampal function. , 1992, Psychological review.

[34]  B. H. Bland,et al.  The Role of the Septohippocampal Pathway in the Regulation of Hippocampal Field Activity and Behavior: Analysis by the Intraseptal Microinfusion of Carbachol, Atropine, and Procaine , 1993, Experimental Neurology.

[35]  S. D. Berry,et al.  Hippocampal plasticity during jaw movement conditioning in the rabbit , 1993, Brain Research.

[36]  W. Singer.  Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[37]  M. Fanselow,et al.  Parallel augmentation of hippocampal long-term potentiation, theta rhythm, and contextual fear conditioning in water-deprived rats. , 1994, Behavioral neuroscience.

[38]  I. Kirk,et al.  Classification of theta‐related cells in the entorhinal cortex: Cell discharges are controlled by the ascending brainstem synchronizing pathway in parallel with hippocampal theta‐related cells , 1995, Hippocampus.

[39]  D. Olton,et al.  Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  M. Hasselmo,et al.  A Computational Model of Cholinergic Disruption of Septohippocampal Activity in Classical Eyeblink Conditioning , 1996, Neurobiology of Learning and Memory.

[41]  Lucien T. Thompson,et al.  Trace eyeblink conditioning in rabbits demonstrates heterogeneity of learning ability both between and within age groups , 1996, Neurobiology of Aging.

[42]  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.

[43]  M. Gluck,et al.  Psychobiological models of hippocampal function in learning and memory. , 1997, Annual review of psychology.

[44]  T. Kaneko,et al.  Disruption of trace conditioning of the nictitating membrane response in rabbits by central cholinergic blockade , 1997, Psychopharmacology.

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

[46]  Mark J. Thomas,et al.  Postsynaptic Complex Spike Bursting Enables the Induction of LTP by Theta Frequency Synaptic Stimulation , 1998, The Journal of Neuroscience.

[47]  J F Disterhoft,et al.  Hippocampal encoding of non‐spatial trace conditioning , 1999, Hippocampus.

[48]  D. Woodruff-Pak.  New Directions For a Classical Paradigm: Human Eyeblink Conditioning , 1999 .

[49]  R. Clark,et al.  Awareness predicts the magnitude of single‐cue trace eyeblink conditioning , 2000, Hippocampus.

[50]  J. Karhu,et al.  Theta oscillations index human hippocampal activation during a working memory task. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[51]  S. D. Berry,et al.  Medial septal microinfusion of scopolamine disrupts hippocampal activity and trace jaw movement conditioning. , 2000, Behavioral neuroscience.

[52]  S. Raghavachari,et al.  Gating of Human Theta Oscillations by a Working Memory Task , 2001, The Journal of Neuroscience.

[53]  M. Kahana,et al.  Theta returns , 2001, Current Opinion in Neurobiology.

[54]  G. V. Prisco,et al.  Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez’s circuit , 2001, Neuroscience.

[55]  L. Jarrard,et al.  The hippocampus and motivation revisited: appetite and activity , 2001, Behavioural Brain Research.

[56]  A. David Redish,et al.  The hippocampal debate: are we asking the right questions? , 2001, Behavioural Brain Research.

[57]  S. Raghavachari,et al.  Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. , 2001, Journal of neurophysiology.

[58]  S. D. Berry,et al.  Hippocampal Theta Oscillations and Classical Conditioning , 2001, Neurobiology of Learning and Memory.

[59]  L M Frank,et al.  A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. , 2001, Journal of neurophysiology.

[60]  S. D. Berry,et al.  Motivational Issues in Aversive and Appetitive Conditioning Paradigms , 2002 .

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

[62]  Michael E. Hasselmo,et al.  A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning , 2002, Neural Computation.

[63]  S. D. Berry,et al.  Oscillatory brain states and learning: Impact of hippocampal theta-contingent training , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[64]  S. D. Berry,et al.  Reversible septal inactivation disrupts hippocampal slow-wave and unit activity and impairs trace conditioning in rabbits (Oryctolagus cuniculus). , 2002, Behavioral neuroscience.