Plasticity of the synaptic modification range.

Activity-dependent synaptic plasticity is likely to provide a mechanism for learning and memory. Cortical synaptic responses that are strengthened within a fixed synaptic modification range after 5 days of motor skill learning are driven near the top of their range, leaving only limited room for additional synaptic strengthening. If synaptic strengthening is a requisite step for acquiring new skills, near saturation of long-term potentiation (LTP) should impede further learning or the LTP mechanism should recover after single-task learning. Here we show that the initial learning-induced synaptic enhancement is sustained even long after training has been discontinued and that the synaptic modification range shifts upward. This range shift places increased baseline synaptic efficacy back within the middle of its operating range, allowing prelearning levels of LTP and long-term depression. Persistent synaptic strengthening might be a substrate for long-term retention in motor cortex, whereas the shift in synaptic modification range ensures the availability for new synaptic strengthening.

[1]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  B L McNaughton,et al.  Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  C. A. Castro,et al.  Recovery of spatial learning deficits after decay of electrically induced synaptic enhancement in the hippocampus , 1989, Nature.

[4]  P. Milner A cell assembly theory of hippocampal amnesia , 1989, Neuropsychologia.

[5]  S. Aou,et al.  Increases in excitability of neurons of the motor cortex of cats after rapid acquisition of eye blink conditioning , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  P. Andersen,et al.  Synaptic potentiation in the rat dentate gyrus during exploratory learning. , 1993, Neuroreport.

[7]  B L McNaughton,et al.  LTP saturation and spatial learning disruption: effects of task variables and saturation levels , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  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.

[9]  J. Isaac,et al.  Evidence for silent synapses: Implications for the expression of LTP , 1995, Neuron.

[10]  R. Malinow,et al.  Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice , 1995, Nature.

[11]  Norton W. Milgram,et al.  Post-activation potentiation in the neocortex. IV. Multiple sessions required for induction of long-term potentiation in the chronic preparation , 1995, Brain Research.

[12]  K. Miller,et al.  Synaptic Economics: Competition and Cooperation in Synaptic Plasticity , 1996, Neuron.

[13]  J. Disterhoft,et al.  Trace Eyeblink Conditioning Increases CA1 Excitability in a Transient and Learning-Specific Manner , 1996, The Journal of Neuroscience.

[14]  J F Disterhoft,et al.  Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. , 1996, Journal of neurophysiology.

[15]  M. McKERNAN,et al.  Fear conditioning induces a lasting potentiation of synaptic currents in vitro , 1997, Nature.

[16]  T. Brashers-Krug,et al.  Functional Stages in the Formation of Human Long-Term Motor Memory , 1997, The Journal of Neuroscience.

[17]  Joseph E LeDoux,et al.  Fear conditioning induces associative long-term potentiation in the amygdala , 1997, Nature.

[18]  Peter Somogyi,et al.  Cell Type and Pathway Dependence of Synaptic AMPA Receptor Number and Variability in the Hippocampus , 1998, Neuron.

[19]  R. Racine,et al.  Long-term potentiation in the neocortex of the adult, freely moving rat. , 1998, Cerebral cortex.

[20]  R. Morris,et al.  Impaired spatial learning after saturation of long-term potentiation. , 1998, Science.

[21]  J. Morrison,et al.  Synaptic coexistence of AMPA and NMDA receptors in the rat hippocampus: A postembedding immunogold study , 1998, Journal of neuroscience research.

[22]  J. Donoghue,et al.  Strengthening of horizontal cortical connections following skill learning , 1998, Nature Neuroscience.

[23]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[24]  G. Turrigiano Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same , 1999, Trends in Neurosciences.

[25]  F. Roman,et al.  Correlations between electrophysiological observations of synaptic plasticity modifications and behavioral performance in mammals , 1999, Progress in Neurobiology.

[26]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[27]  M. Carandini,et al.  Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. , 2000, Journal of neurophysiology.

[28]  S. Nelson,et al.  Hebb and homeostasis in neuronal plasticity , 2000, Current Opinion in Neurobiology.

[29]  R. Nicoll,et al.  Synaptic plasticity and dynamic modulation of the postsynaptic membrane , 2000, Nature Neuroscience.

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

[31]  S. J. Martin,et al.  Synaptic plasticity and memory: an evaluation of the hypothesis. , 2000, Annual review of neuroscience.

[32]  C Bucherelli,et al.  Long‐lasting hippocampal potentiation and contextual memory consolidation , 2001, The European journal of neuroscience.

[33]  S. J. Martin,et al.  Cortical plasticity: It's all the range! , 2001, Current Biology.

[34]  J. Kleim,et al.  Motor Learning-Dependent Synaptogenesis Is Localized to Functionally Reorganized Motor Cortex , 2002, Neurobiology of Learning and Memory.

[35]  S. J. Martin,et al.  New life in an old idea: The synaptic plasticity and memory hypothesis revisited , 2002, Hippocampus.

[36]  A. Keller Use-dependent inhibition of dendritic spines , 2002, Trends in Neurosciences.

[37]  G. Knott,et al.  Formation of Dendritic Spines with GABAergic Synapses Induced by Whisker Stimulation in Adult Mice , 2002, Neuron.

[38]  R. Malenka Synaptic Plasticity and AMPA Receptor Trafficking , 2003, Annals of the New York Academy of Sciences.

[39]  W. Abraham How long will long-term potentiation last? , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[41]  D. Ruge,et al.  Learning Modifies Subsequent Induction of Long-Term Potentiation-Like and Long-Term Depression-Like Plasticity in Human Motor Cortex , 2004, The Journal of Neuroscience.

[42]  G. Teskey,et al.  Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation , 2004, Neuroscience.

[43]  Jeremy D. Cohen,et al.  Skilled motor learning does not enhance long-term depression in the motor cortex in vivo. , 2005, Journal of neurophysiology.

[44]  R. A. Hodgson,et al.  Training-induced and electrically induced potentiation in the neocortex , 2005, Neurobiology of Learning and Memory.

[45]  Agnès Gruart,et al.  Involvement of the CA3–CA1 Synapse in the Acquisition of Associative Learning in Behaving Mice , 2006, The Journal of Neuroscience.

[46]  Jonathan R. Whitlock,et al.  Learning Induces Long-Term Potentiation in the Hippocampus , 2006, Science.

[47]  Tobias Bonhoeffer,et al.  Homeostatic shutdown of long-term potentiation in the adult hippocampus. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[48]  A. Dunaevsky,et al.  Dendritic spine plasticity: Looking beyond development , 2007, Brain Research.

[49]  T. Soderling,et al.  Regulatory mechanisms of AMPA receptors in synaptic plasticity , 2007, Nature Reviews Neuroscience.