Functional Impact of Dendritic Branch-Point Morphology

Cortical pyramidal cells store multiple features of complex synaptic input in individual dendritic branches and independently regulate the coupling between dendritic and somatic spikes. Branch points in apical trees exhibit wide ranges of sizes and shapes, and the large diameter ratio between trunk and oblique dendrites exacerbates impedance mismatch. The morphological diversity of dendritic bifurcations could thus locally tune neuronal excitability and signal integration. However, these aspects have never been investigated. Here, we first quantified the morphological variability of branch points from two-photon images of rat CA1 pyramidal neurons. We then investigated the geometrical features affecting spike initiation, propagation, and timing with a computational model validated by glutamate uncaging experiments. The results suggest that even subtle membrane readjustments at branch points could drastically alter the ability of synaptic input to generate, propagate, and time action potentials.

[1]  V. Murthy,et al.  Experience-Dependent Modification of Primary Sensory Synapses in the Mammalian Olfactory Bulb , 2007, The Journal of Neuroscience.

[2]  Kenji Morita Possible Role of Dendritic Compartmentalization in the Spatial Working Memory Circuit , 2008, The Journal of Neuroscience.

[3]  Mriganka Sur,et al.  Structural Dynamics of Synapses in Vivo Correlate with Functional Changes during Experience-Dependent Plasticity in Visual Cortex , 2010, The Journal of Neuroscience.

[4]  Giorgio A. Ascoli,et al.  Computational simulation of the input-output relationship in hippocampal pyramidal cells , 2006, Journal of Computational Neuroscience.

[5]  Giorgio A Ascoli,et al.  Signal propagation in oblique dendrites of CA1 pyramidal cells. , 2005, Journal of neurophysiology.

[6]  Kristen M. Harris,et al.  Plasticity-Induced Growth of Dendritic Spines by Exocytic Trafficking from Recycling Endosomes , 2006, Neuron.

[7]  D. Johnston,et al.  Active dendrites: colorful wings of the mysterious butterflies , 2008, Trends in Neurosciences.

[8]  J. Bourne,et al.  Local Zones of Endoplasmic Reticulum Complexity Confine Cargo in Neuronal Dendrites , 2012, Cell.

[9]  Erin M. Schuman,et al.  Frontiers in Cellular Neuroscience Cellular Neuroscience , 2022 .

[10]  Y. Zuo,et al.  Experience-dependent structural plasticity in the cortex , 2011, Trends in Neurosciences.

[11]  J. Magee,et al.  On the Initiation and Propagation of Dendritic Spikes in CA1 Pyramidal Neurons , 2004, The Journal of Neuroscience.

[12]  Qian-Quan Sun,et al.  Experience-dependent intrinsic plasticity in interneurons of barrel cortex layer IV. , 2009, Journal of neurophysiology.

[13]  G. Ascoli,et al.  Quantitative morphometry of hippocampal pyramidal cells: Differences between anatomical classes and reconstructing laboratories , 2004, The Journal of comparative neurology.

[14]  Dejan Zecevic,et al.  Dendritic signals from rat hippocampal CA1 pyramidal neurons during coincident pre‐ and post‐synaptic activity: a combined voltage‐ and calcium‐imaging study , 2007, The Journal of physiology.

[15]  Bartlett W. Mel,et al.  Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue , 2001, Neuron.

[16]  D. Johnston,et al.  K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons , 1997, Nature.

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

[18]  Andreas T. Schaefer,et al.  Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. , 2003, Journal of neurophysiology.

[19]  J. Magee,et al.  Distance-Dependent Increase in AMPA Receptor Number in the Dendrites of Adult Hippocampal CA1 Pyramidal Neurons , 2001, The Journal of Neuroscience.

[20]  Idan Segev,et al.  The interplay between homeostatic synaptic plasticity and functional dendritic compartments. , 2006, Journal of neurophysiology.

[21]  D. Hoffman,et al.  DPP6 Establishes the A-Type K+ Current Gradient Critical for the Regulation of Dendritic Excitability in CA1 Hippocampal Neurons , 2011, Neuron.

[22]  J. Magee,et al.  Integrative Properties of Radial Oblique Dendrites in Hippocampal CA1 Pyramidal Neurons , 2006, Neuron.

[23]  D. Alkon,et al.  Memory and long-term potentiation (LTP) dissociated: normal spatial memory despite CA1 LTP elimination with Kv1.4 antisense. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Bourne,et al.  Balancing structure and function at hippocampal dendritic spines. , 2008, Annual review of neuroscience.

[25]  Yi Zuo,et al.  Spine Neck Plasticity Controls Postsynaptic Calcium Signals through Electrical Compartmentalization , 2008, The Journal of Neuroscience.

[26]  Michele Migliore,et al.  Normalization of Ca2+ Signals by Small Oblique Dendrites of CA1 Pyramidal Neurons , 2003, The Journal of Neuroscience.

[27]  Masaki Nomura,et al.  Conserved properties of dendritic trees in four cortical interneuron subtypes , 2011, Scientific reports.

[28]  G. Ascoli,et al.  Dendritic excitability and neuronal morphology as determinants of synaptic efficacy. , 2009, Journal of neurophysiology.

[29]  Judit K. Makara,et al.  Compartmentalized dendritic plasticity and input feature storage in neurons , 2008, Nature.

[30]  Stuart D. Washington,et al.  Effects of dendritic morphology on CA3 pyramidal cell electrophysiology: a simulation study , 2002, Brain Research.

[31]  Michele Migliore,et al.  Normalization of Ca 2 Signals by Small Oblique Dendrites of CA 1 Pyramidal Neurons , 2003 .

[32]  N. Spruston,et al.  Synapse Distribution Suggests a Two-Stage Model of Dendritic Integration in CA1 Pyramidal Neurons , 2009, Neuron.

[33]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[34]  E. Marder,et al.  Activity-dependent changes in the intrinsic properties of cultured neurons. , 1994, Science.

[35]  Michele Migliore,et al.  Dendritic Ih Selectively Blocks Temporal Summation of Unsynchronized Distal Inputs in CA1 Pyramidal Neurons , 2004, Journal of Computational Neuroscience.

[36]  Nace L. Golding,et al.  Dendritic Sodium Spikes Are Variable Triggers of Axonal Action Potentials in Hippocampal CA1 Pyramidal Neurons , 1998, Neuron.

[37]  Scott M Thompson,et al.  Unique roles of SK and Kv4.2 potassium channels in dendritic integration. , 2004, Neuron.

[38]  Jozsef Csicsvari,et al.  Activity-Dependent Control of Neuronal Output by Local and Global Dendritic Spike Attenuation , 2009, Neuron.

[39]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[40]  D. Hoffman,et al.  Dendritic ion channel trafficking and plasticity , 2010, Trends in Neurosciences.

[41]  Giorgio A Ascoli,et al.  Computational models of neuronal biophysics and the characterization of potential neuropharmacological targets. , 2008, Current medicinal chemistry.

[42]  T. Sejnowski,et al.  [Letters to nature] , 1996, Nature.

[43]  Matthew F. Nolan,et al.  A Behavioral Role for Dendritic Integration HCN1 Channels Constrain Spatial Memory and Plasticity at Inputs to Distal Dendrites of CA1 Pyramidal Neurons , 2004, Cell.

[44]  Judit K. Makara,et al.  Experience-dependent compartmentalized dendritic plasticity in rat hippocampal CA1 pyramidal neurons , 2009, Nature Neuroscience.

[45]  J. Magee Dendritic Hyperpolarization-Activated Currents Modify the Integrative Properties of Hippocampal CA1 Pyramidal Neurons , 1998, The Journal of Neuroscience.