Activity-Dependent Control of Neuronal Output by Local and Global Dendritic Spike Attenuation

Neurons possess elaborate dendritic arbors which receive and integrate excitatory synaptic signals. Individual dendritic subbranches exhibit local membrane potential supralinearities, termed dendritic spikes, which control transfer of local synaptic input to the soma. Here, we show that dendritic spikes in CA1 pyramidal cells are strongly regulated by specific types of prior input. While input in the linear range is without effect, supralinear input inhibits subsequent spikes, causing them to attenuate and ultimately fail due to dendritic Na(+) channel inactivation. This mechanism acts locally within the boundaries of the input branch. If an input is sufficiently strong to trigger axonal action potentials, their back-propagation into the dendritic tree causes a widespread global reduction in dendritic excitability which is prominent after firing patterns occurring in vivo. Together, these mechanisms control the capability of individual dendritic branches to trigger somatic action potential output. They are invoked at frequencies encountered during learning, and impose limits on the storage and retrieval rates of information encoded as branch excitability.

[1]  G. Buzsáki,et al.  Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity‐dependent phase‐precession of action potentials , 1998, Hippocampus.

[2]  A. Polsky,et al.  Submillisecond Precision of the Input-Output Transformation Function Mediated by Fast Sodium Dendritic Spikes in Basal Dendrites of CA1 Pyramidal Neurons , 2003, The Journal of Neuroscience.

[3]  J. O’Neill,et al.  Place-Selective Firing of CA1 Pyramidal Cells during Sharp Wave/Ripple Network Patterns in Exploratory Behavior , 2006, Neuron.

[4]  J. Magee,et al.  State-Dependent Dendritic Computation in Hippocampal CA1 Pyramidal Neurons , 2006, The Journal of Neuroscience.

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

[6]  Johannes J. Letzkus,et al.  Dendritic mechanisms controlling spike-timing-dependent synaptic plasticity , 2007, Trends in Neurosciences.

[7]  Urit Gordon,et al.  Plasticity Compartments in Basal Dendrites of Neocortical Pyramidal Neurons , 2006, The Journal of Neuroscience.

[8]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[9]  B. Kampa,et al.  Calcium Spikes in Basal Dendrites of Layer 5 Pyramidal Neurons during Action Potential Bursts , 2006, The Journal of Neuroscience.

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

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

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

[13]  J. Csicsvari,et al.  Ensemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events , 2000, Neuron.

[14]  D. Johnston,et al.  Slow Recovery from Inactivation of Na+ Channels Underlies the Activity-Dependent Attenuation of Dendritic Action Potentials in Hippocampal CA1 Pyramidal Neurons , 1997, The Journal of Neuroscience.

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

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

[17]  L. Frank,et al.  New Experiences Enhance Coordinated Neural Activity in the Hippocampus , 2008, Neuron.

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

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

[20]  Nace L. Golding,et al.  Compartmental Models Simulating a Dichotomy of Action Potential Backpropagation in Ca1 Pyramidal Neuron Dendrites , 2001, Journal of neurophysiology.

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

[22]  J. Magee,et al.  Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. , 1999, Journal of neurophysiology.

[23]  Leslie M Loew,et al.  Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons , 2008, The European journal of neuroscience.

[24]  A. Polsky,et al.  Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study , 2007, Nature Neuroscience.

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

[26]  Michael Häusser,et al.  Dendritic Calcium Spikes Are Tunable Triggers of Cannabinoid Release and Short-Term Synaptic Plasticity in Cerebellar Purkinje Neurons , 2006, The Journal of Neuroscience.

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

[28]  H. Wigström,et al.  Single high strength afferent volleys can produce long-term potentiation in the hippocampus in vitro , 1986, Neuroscience Letters.

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

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

[31]  M. Häusser,et al.  Initiation and spread of sodium action potentials in cerebellar purkinje cells , 1994, Neuron.

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

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

[34]  N. Spruston,et al.  Prolonged Sodium Channel Inactivation Contributes to Dendritic Action Potential Attenuation in Hippocampal Pyramidal Neurons , 1997, The Journal of Neuroscience.

[35]  S. Hoffman,et al.  Funding for malaria genome sequencing , 1997, Nature.

[36]  R. Yuste,et al.  Linear Summation of Excitatory Inputs by CA1 Pyramidal Neurons , 1999, Neuron.