Behavioral time scale synaptic plasticity underlies CA1 place fields

A different form of synaptic plasticity How do synaptic or other neuronal changes support learning? This subject has been dominated by Hebb's postulate of synaptic change. Although there is strong experimental support for Hebbian plasticity in a number of preparations, alternative ideas have also been developed over the years. Bittner et al. provide in vivo, in vitro, and modeling data to support the view that non-Hebbian plasticity may underlie the formation of hippocampal place fields (see the Perspective by Krupic). Instead of multiple pairings, a single strong Ca2+ plateau potential in neuronal dendrites paired with spatial inputs may be sufficient to produce place cells. Science, this issue p. 1033; see also p. 974 A particular type of long–time scale plasticity shapes the formation of stable place fields in the hippocampus. Learning is primarily mediated by activity-dependent modifications of synaptic strength within neuronal circuits. We discovered that place fields in hippocampal area CA1 are produced by a synaptic potentiation notably different from Hebbian plasticity. Place fields could be produced in vivo in a single trial by potentiation of input that arrived seconds before and after complex spiking. The potentiated synaptic input was not initially coincident with action potentials or depolarization. This rule, named behavioral time scale synaptic plasticity, abruptly modifies inputs that were neither causal nor close in time to postsynaptic activation. In slices, five pairings of subthreshold presynaptic activity and calcium (Ca2+) plateau potentials produced a large potentiation with an asymmetric seconds-long time course. This plasticity efficiently stores entire behavioral sequences within synaptic weights to produce predictive place cell activity.

[1]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[2]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[3]  A G Barto,et al.  Toward a modern theory of adaptive networks: expectation and prediction. , 1981, Psychological review.

[4]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[5]  R. F. Thompson,et al.  Mammalian brain substrates of aversive classical conditioning. , 1993, Annual review of psychology.

[6]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  L. F. Abbott,et al.  A Model of Spatial Map Formation in the Hippocampus of the Rat , 1999, Neural Computation.

[8]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[9]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[10]  C Kentros,et al.  Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. , 1998, Science.

[11]  David J. Foster,et al.  A model of hippocampally dependent navigation, using the temporal difference learning rule , 2000, Hippocampus.

[12]  S. Molden,et al.  Accumulation of Hippocampal Place Fields at the Goal Location in an Annular Watermaze Task , 2001, The Journal of Neuroscience.

[13]  L. Squire Memory systems of the brain: A brief history and current perspective , 2004, Neurobiology of Learning and Memory.

[14]  L. Abbott,et al.  Extending the effects of spike-timing-dependent plasticity to behavioral timescales. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  E. Izhikevich Solving the distal reward problem through linkage of STDP and dopamine signaling , 2007, BMC Neuroscience.

[16]  N. Spruston,et al.  Dendritic spikes induce single-burst long-term potentiation , 2007, Proceedings of the National Academy of Sciences.

[17]  György Buzsáki,et al.  Hippocampal place cell assemblies are speed-controlled oscillators , 2007, Proceedings of the National Academy of Sciences.

[18]  The Spread of Ras Activity Triggered by Activation of a Single Dendritic Spine , 2008, Science.

[19]  D. Tank,et al.  Intracellular dynamics of hippocampal place cells during virtual navigation , 2009, Nature.

[20]  J. Magee,et al.  Pathway Interactions and Synaptic Plasticity in the Dendritic Tuft Regions of CA1 Pyramidal Neurons , 2009, Neuron.

[21]  Seok-Jin R. Lee,et al.  Activation of CaMKII in single dendritic spines during long-term potentiation , 2009, Nature.

[22]  Michael L. Hines,et al.  Neuroinformatics Original Research Article Neuron and Python , 2022 .

[23]  J. O’Neill,et al.  The reorganization and reactivation of hippocampal maps predict spatial memory performance , 2010, Nature Neuroscience.

[24]  Eric R Kandel,et al.  Synapses and memory storage. , 2012, Cold Spring Harbor perspectives in biology.

[25]  G. Laurent,et al.  Conditional modulation of spike-timing-dependent plasticity for olfactory learning , 2012, Nature.

[26]  Kamran Diba,et al.  Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons , 2012, Hippocampus.

[27]  David J. Foster,et al.  Sequence learning and the role of the hippocampus in rodent navigation , 2012, Current Opinion in Neurobiology.

[28]  Doyun Lee,et al.  Hippocampal Place Fields Emerge upon Single-Cell Manipulation of Excitability During Behavior , 2012, Science.

[29]  D. Feldman The Spike-Timing Dependence of Plasticity , 2012, Neuron.

[30]  Brad E. Pfeiffer,et al.  Hippocampal place cell sequences depict future paths to remembered goals , 2013, Nature.

[31]  H. Eichenbaum Time cells in the hippocampus: a new dimension for mapping memories , 2014, Nature Reviews Neuroscience.

[32]  Susumu Tonegawa,et al.  Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons , 2015, Nature Neuroscience.

[33]  R. Tsien,et al.  Sequential ionic and conformational signaling by calcium channels drives neuronal gene expression , 2016, Science.

[34]  Nachum Ulanovsky,et al.  Vectorial representation of spatial goals in the hippocampus of bats , 2017, Science.

[35]  Sandro Romani,et al.  Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in CA1 place cells , 2017, Nature Neuroscience.