Plasticity Compartments in Basal Dendrites of Neocortical Pyramidal Neurons

Synaptic plasticity rules widely determine how cortical networks develop and store information. Using confocal imaging and dual site focal synaptic stimulation, we show that basal dendrites, which receive the majority of synapses innervating neocortical pyramidal neurons, contain two compartments with respect to plasticity rules. Synapses innervating the proximal basal tree are easily modified when paired with the global activity of the neuron. In contrast, synapses innervating the distal basal tree fail to change in response to global suprathreshold activity or local dendritic spikes. These synapses can undergo long-term potentiation under unusual conditions when local NMDA spikes, which evoke large calcium transients, are paired with a “gating molecule,” BDNF. Moreover, these synapses use a new temporal plasticity rule, which is an order of magnitude longer than spike timing dependent plasticity and prefers reversed presynaptic/postsynaptic activation order. The newly described plasticity compartmentalization of basal dendrites expands the networks plasticity rules and may support different learning and developmental functions.

[1]  SECTION H. ANTHROPOLOGY. TITLES FOR PRESENTATION AT THE DENVER MEETING , 1901 .

[2]  D. Pandya,et al.  Architecture and Connections of Cortical Association Areas , 1985 .

[3]  A. Larkman,et al.  Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions , 1991, The Journal of comparative neurology.

[4]  W. Singer,et al.  Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation , 1993, Trends in Neurosciences.

[5]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[6]  Mark F. Bear,et al.  Neocortical long-term potentiation , 1993, Current Opinion in Neurobiology.

[7]  L. Cauller,et al.  Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Mark F. Bear,et al.  Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience , 1995, Nature.

[9]  N. Spruston,et al.  Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. , 1995, Science.

[10]  T Bonhoeffer,et al.  Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Michael C. Crair,et al.  A critical period for long-term potentiation at thalamocortical synapses , 1995, Nature.

[12]  T. Bonhoeffer Neurotrophins and activity-dependent development of the neocortex , 1996, Current Opinion in Neurobiology.

[13]  T Bonhoeffer,et al.  Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  E. Welker,et al.  Upregulation of BDNF mRNA Expression in the Barrel Cortex of Adult Mice after Sensory Stimulation , 1996, The Journal of Neuroscience.

[15]  E. Schuman,et al.  Neurotrophins and Time: Different Roles for TrkB Signaling in Hippocampal Long-Term Potentiation , 1997, Neuron.

[16]  N. Seidah,et al.  Regulation by gastric acid of the processing of progastrin‐derived peptides in rat antral mucosa , 1997, The Journal of physiology.

[17]  B. Sakmann,et al.  Action potential initiation and propagation in rat neocortical pyramidal neurons , 1997, The Journal of physiology.

[18]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[19]  D. Johnston,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997 .

[20]  B. Sakmann,et al.  Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons , 1997, The Journal of physiology.

[21]  T. Reader,et al.  Functional Evidence that BDNF Is an Anterograde Neuronal Trophic Factor in the CNS , 1998, The Journal of Neuroscience.

[22]  B. Sakmann,et al.  Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Borst,et al.  Dendritic integration and its role in computing image velocity. , 1998, Science.

[24]  C. Altar,et al.  Neurotrophin trafficking by anterograde transport , 1998, Trends in Neurosciences.

[25]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[26]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[27]  Timing of cochlear feedback: spatial and temporal representation of a tone across the basilar membrane , 1999, Nature Neuroscience.

[28]  J. Magee Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons , 1999, Nature Neuroscience.

[29]  O. Paulsen,et al.  Rapid report: postsynaptic bursting is essential for 'Hebbian' induction of associative long-term potentiation at excitatory synapses in rat hippocampus. , 1999, The Journal of physiology.

[30]  E. Schuman Neurotrophin regulation of synaptic transmission , 1999, Current Opinion in Neurobiology.

[31]  I. Black,et al.  Trophic regulation of synaptic plasticity. , 1999, Journal of neurobiology.

[32]  B. Sakmann,et al.  Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Tobias Bonhoeffer,et al.  Essential Role for TrkB Receptors in Hippocampus-Mediated Learning , 1999, Neuron.

[34]  M Migliore,et al.  Dendritic potassium channels in hippocampal pyramidal neurons , 2000, The Journal of physiology.

[35]  B. Sakmann,et al.  Voltage‐gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients , 2000, The Journal of physiology.

[36]  J. Schiller,et al.  NMDA spikes in basal dendrites of cortical pyramidal neurons , 2000, Nature.

[37]  T. Sejnowski,et al.  Natural patterns of activity and long-term synaptic plasticity , 2000, Current Opinion in Neurobiology.

[38]  J. Magee Dendritic integration of excitatory synaptic input , 2000, Nature Reviews Neuroscience.

[39]  E. Levine,et al.  Brain‐derived neurotrophic factor increases activity of NR2B‐containing N‐methyl‐D‐aspartate receptors in excised patches from hippocampal neurons , 2000, Journal of neuroscience research.

[40]  D. Feldman,et al.  Timing-Based LTP and LTD at Vertical Inputs to Layer II/III Pyramidal Cells in Rat Barrel Cortex , 2000, Neuron.

[41]  Mu-ming Poo,et al.  The neurotrophin hypothesis for synaptic plasticity , 2000, Trends in Neurosciences.

[42]  Y. Ishikawa,et al.  Biological characterization and optical imaging of brain‐derived neurotrophic factor‐green fluorescent protein suggest an activity‐dependent local release of brain‐derived neurotrophic factor in neurites of cultured hippocampal neurons , 2001, Journal of neuroscience research.

[43]  T. Tsumoto,et al.  Activity-Dependent Transfer of Brain-Derived Neurotrophic Factor to Postsynaptic Neurons , 2001, Science.

[44]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

[45]  T. Freund,et al.  Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells , 2001, Neuroscience.

[46]  R. Heumann,et al.  Synaptic secretion of BDNF after high‐frequency stimulation of glutamatergic synapses , 2001, The EMBO journal.

[47]  A. Konnerth,et al.  Neurotrophin-evoked depolarization requires the sodium channel NaV1.9 , 2002, Nature.

[48]  Arthur Konnerth,et al.  Postsynaptic Induction of BDNF-Mediated Long-Term Potentiation , 2002, Science.

[49]  P. J. Sjöström,et al.  Spike timing, calcium signals and synaptic plasticity , 2002, Current Opinion in Neurobiology.

[50]  Terrence J Sejnowski,et al.  Complexity of calcium signaling in synaptic spines. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[51]  Nace L. Golding,et al.  Dendritic spikes as a mechanism for cooperative long-term potentiation , 2002, Nature.

[52]  P. Detwiler,et al.  Directionally selective calcium signals in dendrites of starburst amacrine cells , 2002, Nature.

[53]  R. Silver,et al.  Synaptic connections between layer 4 spiny neurone‐ layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column , 2002, The Journal of physiology.

[54]  E. Huang,et al.  Trk receptors: roles in neuronal signal transduction. , 2003, Annual review of biochemistry.

[55]  Volkmar Lessmann,et al.  Neurotrophin secretion: current facts and future prospects , 2003, Progress in Neurobiology.

[56]  Bartlett W. Mel,et al.  Dendrites: bug or feature? , 2003, Current Opinion in Neurobiology.

[57]  G. Collingridge,et al.  Differential Roles of NR2A and NR2B-Containing NMDA Receptors in Cortical Long-Term Potentiation and Long-Term Depression , 2004, The Journal of Neuroscience.

[58]  Michele Migliore,et al.  Role of an A-Type K+ Conductance in the Back-Propagation of Action Potentials in the Dendrites of Hippocampal Pyramidal Neurons , 1999, Journal of Computational Neuroscience.

[59]  L. Maler,et al.  Plastic and Nonplastic Pyramidal Cells Perform Unique Roles in a Network Capable of Adaptive Redundancy Reduction , 2004, Neuron.

[60]  Y. Dan,et al.  Spike Timing-Dependent Plasticity of Neural Circuits , 2004, Neuron.

[61]  Spartaco Santi,et al.  Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[62]  K. Holthoff,et al.  Single‐shock LTD by local dendritic spikes in pyramidal neurons of mouse visual cortex , 2004, The Journal of physiology.

[63]  Mu-ming Poo,et al.  Rapid BDNF-induced retrograde synaptic modification in a developing retinotectal system , 2004, Nature.

[64]  M. Sheng,et al.  Role of NMDA Receptor Subtypes in Governing the Direction of Hippocampal Synaptic Plasticity , 2004, Science.

[65]  H. Scharfman,et al.  Brain-derived neurotrophic factor. , 2004, Growth factors.

[66]  Bartlett W. Mel,et al.  Computational subunits in thin dendrites of pyramidal cells , 2004, Nature Neuroscience.

[67]  Y. Dan,et al.  Spike-timing-dependent synaptic plasticity depends on dendritic location , 2005, Nature.

[68]  T. Tsumoto,et al.  Difference in trafficking of brain-derived neurotrophic factor between axons and dendrites of cortical neurons, revealed by live-cell imaging , 2005, BMC Neuroscience.

[69]  J. DeFelipe,et al.  Catecholaminergic innervation of pyramidal neurons in the human temporal cortex. , 2005, Cerebral cortex.

[70]  N. Spruston,et al.  Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity , 2005, Nature Neuroscience.

[71]  C. Bramham,et al.  BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis , 2005, Progress in Neurobiology.

[72]  Johannes J. Letzkus,et al.  Learning Rules for Spike Timing-Dependent Plasticity Depend on Dendritic Synapse Location , 2006, The Journal of Neuroscience.

[73]  P. J. Sjöström,et al.  A Cooperative Switch Determines the Sign of Synaptic Plasticity in Distal Dendrites of Neocortical Pyramidal Neurons , 2006, Neuron.