Temporal Properties of Cerebellar-Dependent Memory Consolidation

Classical conditioning of the nictitating membrane response in rabbits is a well defined model of cerebellar-dependent motor memory. This memory undergoes a period of consolidation after the training session, when it is sensitive to reversible inactivations of the cerebellar cortex, but not of the cerebellar nuclei, with the GABAA receptor agonist muscimol. Here, the temporal properties of this cerebellar cortex-dependent consolidation were examined using delayed infusions of muscimol in cortical lobule HVI. Cortical infusions delayed by 5 or 45 min after a conditioning session produced significant and very similar impairments of consolidation, but infusions delayed by 90 min produced little or no impairment. Behavioral measures indicate that the muscimol infusions produced significant effects after ∼30 min and they lasted for a few hours. So, over a time window beginning ∼1 hr after the end of the training session and closing 1 hr after that, intracortical activity is critical for consolidation of this motor memory.

[1]  Narender Ramnani,et al.  Reversible inactivations of the cerebellum with muscimol prevent the acquisition and extinction of conditioned nictitating membrane responses in the rabbit , 1996, Experimental Brain Research.

[2]  M. Garwicz,et al.  Evidence for a GABA-mediated cerebellar inhibition of the inferior olive in the cat , 2004, Experimental Brain Research.

[3]  C. Yeo,et al.  Cerebellar cortex and eyeblink conditioning: A reexamination , 2004, Experimental Brain Research.

[4]  D. Linden From Molecules to Memory in the Cerebellum , 2003, Science.

[5]  H. C. Hulscher,et al.  Cerebellar LTD and Learning-Dependent Timing of Conditioned Eyelid Responses , 2003, Science.

[6]  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.

[7]  D. Linden Neuroscience. From molecules to memory in the cerebellum. , 2003, Science.

[8]  Magnus Ivarsson,et al.  Cerebellar Mechanisms in Eyeblink Conditioning , 2002, Annals of the New York Academy of Sciences.

[9]  John H Freeman,et al.  Synapse formation is associated with memory storage in the cerebellum , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  T. Woolsey,et al.  A method to measure the effective spread of focally injected muscimol into the central nervous system with electrophysiology and light microscopy , 2002, Journal of Neuroscience Methods.

[11]  Christopher H. Yeo,et al.  Cerebellar Function in Consolidation of a Motor Memory , 2002, Neuron.

[12]  Henrik Jörntell,et al.  Reciprocal Bidirectional Plasticity of Parallel Fiber Receptive Fields in Cerebellar Purkinje Cells and Their Afferent Interneurons , 2002, Neuron.

[13]  Richard F. Thompson,et al.  Cerebellar cortical inhibition and classical eyeblink conditioning , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  C. Yeo,et al.  Acquisition of Eyeblink Conditioning Is Critically Dependent on Normal Function in Cerebellar Cortical Lobule HVI , 2001, The Journal of Neuroscience.

[15]  M. Mauk,et al.  A Mechanism for Savings in the Cerebellum , 2001, The Journal of Neuroscience.

[16]  E. D’Angelo,et al.  Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum , 2001, Nature Neuroscience.

[17]  V Taglietti,et al.  Theta-Frequency Bursting and Resonance in Cerebellar Granule Cells: Experimental Evidence and Modeling of a Slow K+-Dependent Mechanism , 2001, The Journal of Neuroscience.

[18]  E. Shimizu,et al.  NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. , 2000, Science.

[19]  Joseph E LeDoux,et al.  Memory Consolidation of Auditory Pavlovian Fear Conditioning Requires Protein Synthesis and Protein Kinase A in the Amygdala , 2000, The Journal of Neuroscience.

[20]  Javier F. Medina,et al.  Timing Mechanisms in the Cerebellum: Testing Predictions of a Large-Scale Computer Simulation , 2000, The Journal of Neuroscience.

[21]  D. Linden,et al.  Use-dependent changes in synaptic strength at the Purkinje cell to deep nuclear synapse. , 2000, Progress in brain research.

[22]  Richard F. Thompson,et al.  Learning Induces a CDC2-Related Protein Kinase, KKIAMRE , 1999, The Journal of Neuroscience.

[23]  S. J. Martin,et al.  Reversible neural inactivation reveals hippocampal participation in several memory processes , 1999, Nature Neuroscience.

[24]  J. Raymond Learning in the oculomotor system: from molecules to behavior , 1998, Current Opinion in Neurobiology.

[25]  J. Harvey,et al.  Acute inactivation of the inferior olive blocks associative learning , 1998, The European journal of neuroscience.

[26]  D. Linden,et al.  Polarity of Long-Term Synaptic Gain Change Is Related to Postsynaptic Spike Firing at a Cerebellar Inhibitory Synapse , 1998, Neuron.

[27]  M. Glickstein,et al.  The anatomy of the cerebellum , 1998, Trends in Neurosciences.

[28]  Germund Hesslow,et al.  Cerebellum and conditioned reflexes , 1998, Trends in Cognitive Sciences.

[29]  G Buzsáki,et al.  Memory consolidation during sleep: a neurophysiological perspective. , 1998, Journal of sleep research.

[30]  M. Mauk,et al.  Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses , 1998, Neuropharmacology.

[31]  James R. Bloedel,et al.  Microinjections of anisomycin into the intermediate cerebellum during learning affect the acquisition of classically conditioned responses in the rabbit , 1998, Brain Research.

[32]  E. Bizzi,et al.  Consolidation in human motor memory , 1996, Nature.

[33]  S. Lisberger,et al.  The Cerebellum: A Neuronal Learning Machine? , 1996, Science.

[34]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[35]  Y. Zhang,et al.  Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. I. General properties in comparison with flocculus projecting neurons. , 1995, Journal of neurophysiology.

[36]  S. Highstein,et al.  Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. II. Signal components revealed by reversible flocculus inactivation. , 1995, Journal of neurophysiology.

[37]  A. Scholey,et al.  Two Time Windows of Anisomycin-Induced Amnesia for Passive Avoidance Training in the Day-Old Chick , 1995, Neurobiology of Learning and Memory.

[38]  Richard F. Thompson,et al.  Localization of a memory trace in the mammalian brain. , 1993, Science.

[39]  M. Mauk,et al.  Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  M. J. Scavio,et al.  Posttraining effects of amphetamine, chlorpromazine, ketamine, and scopolamine on the acquisition and extinction of the rabbit's conditioned nictitating membrane response. , 1992, Behavioral neuroscience.

[41]  R. S. Jones The NMDA receptor Edited by J. C. Watkins and G. L. Collinridge. Oxford University Press, New York (1990) 242 pp. £45.00 , 1991, Neuroscience.

[42]  D. Powell,et al.  Naloxone induces multiple effects on aversive Pavlovian conditioning in rabbits. , 1983, Behavioral neuroscience.

[43]  M. Ito Cerebellar control of the vestibulo-ocular reflex--around the flocculus hypothesis. , 1982, Annual review of neuroscience.

[44]  F. A. Miles,et al.  Plasticity in the vestibulo-ocular reflex: a new hypothesis. , 1981, Annual review of neuroscience.

[45]  P. Gilbert How the cerebellum could memorise movements , 1975, Nature.

[46]  J. Albus A Theory of Cerebellar Function , 1971 .

[47]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[48]  I. Gormezano,et al.  Nictitating Membrane: Classical Conditioning and Extinction in the Albino Rabbit , 1962, Science.

[49]  Perla b. Ephrussi Experimentelle Beiträge zur Lehre vom Gedächtnis , 1904 .

[50]  G. Müller,et al.  Experimentelle Beiträge zur Lehre vom Gedächtniss , 1900 .