Potassium Channels Control the Interaction between Active Dendritic Integration Compartments in Layer 5 Cortical Pyramidal Neurons

Active dendritic synaptic integration enhances the computational power of neurons. Such nonlinear processing generates an object-localization signal in the apical dendritic tuft of layer 5B cortical pyramidal neurons during sensory-motor behavior. Here, we employ electrophysiological and optical approaches in brain slices and behaving animals to investigate how excitatory synaptic input to this distal dendritic compartment influences neuronal output. We find that active dendritic integration throughout the apical dendritic tuft is highly compartmentalized by voltage-gated potassium (KV) channels. A high density of both transient and sustained KV channels was observed in all apical dendritic compartments. These channels potently regulated the interaction between apical dendritic tuft, trunk, and axosomatic integration zones to control neuronal output in vitro as well as the engagement of dendritic nonlinear processing in vivo during sensory-motor behavior. Thus, KV channels dynamically tune the interaction between active dendritic integration compartments in layer 5B pyramidal neurons to shape behaviorally relevant neuronal computations.

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

[2]  B. Sakmann,et al.  High frequency action potential bursts (≥ 100 Hz) in L2/3 and L5B thick tufted neurons in anaesthetized and awake rat primary somatosensory cortex , 2008, The Journal of physiology.

[3]  J M Bekkers,et al.  Distribution and activation of voltage‐gated potassium channels in cell‐attached and outside‐out patches from large layer 5 cortical pyramidal neurons of the rat , 2000, The Journal of physiology.

[4]  Stephen R Williams,et al.  Encoding and Decoding of Dendritic Excitation during Active States in Pyramidal Neurons , 2005, The Journal of Neuroscience.

[5]  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.

[6]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

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

[8]  D. Johnston,et al.  Downregulation of Transient K+ Channels in Dendrites of Hippocampal CA1 Pyramidal Neurons by Activation of PKA and PKC , 1998, The Journal of Neuroscience.

[9]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[10]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[12]  Bruce R. Blazar,et al.  Dendritic Discrimination of Temporal Input Sequences in Cortical Neurons , 2010 .

[13]  B. Sakmann,et al.  Dimensions of a Projection Column and Architecture of VPM and POm Axons in Rat Vibrissal Cortex , 2010, Cerebral cortex.

[14]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[15]  Susan E Atkinson,et al.  Pathway‐specific use‐dependent dynamics of excitatory synaptic transmission in rat intracortical circuits , 2007, The Journal of physiology.

[16]  S. Nattel,et al.  Effects of ambasilide, quinidine, flecainide and verapamil on ultra-rapid delayed rectifier potassium currents in canine atrial myocytes. , 2000, Cardiovascular research.

[17]  Celine Mateo,et al.  Motor Control by Sensory Cortex , 2010, Science.

[18]  Beat Lutz,et al.  Synaptic Integration in Tuft Dendrites of Layer 5 Pyramidal Neurons : A New Unifying Principle , 2009 .

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

[20]  Peter Jonas,et al.  Presynaptic Action Potential Amplification by Voltage-Gated Na+ Channels in Hippocampal Mossy Fiber Boutons , 2005, Neuron.

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

[22]  K. Svoboda,et al.  Neural Activity in Barrel Cortex Underlying Vibrissa-Based Object Localization in Mice , 2010, Neuron.

[23]  G. Stuart,et al.  Dependence of EPSP Efficacy on Synapse Location in Neocortical Pyramidal Neurons , 2002, Science.

[24]  Stephen R. Williams,et al.  Postnatal development of dendritic synaptic integration in rat neocortical pyramidal neurons. , 2009, Journal of neurophysiology.

[25]  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.

[26]  Stephen R. Williams,et al.  Spatial compartmentalization and functional impact of conductance in pyramidal neurons , 2004, Nature Neuroscience.

[27]  K. Svoboda,et al.  The subcellular organization of neocortical excitatory connections , 2009, Nature.

[28]  J M Bekkers,et al.  Properties of voltage‐gated potassium currents in nucleated patches from large layer 5 cortical pyramidal neurons of the rat , 2000, The Journal of physiology.

[29]  D. Johnston,et al.  Neuromodulation of dendritic action potentials. , 1999, Journal of neurophysiology.

[30]  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.

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

[32]  R. Nicoll,et al.  Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. , 1990, Physiological reviews.

[33]  C. Gilbert,et al.  Brain States: Top-Down Influences in Sensory Processing , 2007, Neuron.

[34]  M. Larkum,et al.  Signaling of Layer 1 and Whisker-Evoked Ca2+ and Na+ Action Potentials in Distal and Terminal Dendrites of Rat Neocortical Pyramidal Neurons In Vitro and In Vivo , 2002, The Journal of Neuroscience.

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

[36]  W. Giles,et al.  Quinidine-induced inhibition of transient outward current in cardiac muscle. , 1987, The American journal of physiology.

[37]  Nace L. Golding,et al.  Dendritic Calcium Spike Initiation and Repolarization Are Controlled by Distinct Potassium Channel Subtypes in CA1 Pyramidal Neurons , 1999, The Journal of Neuroscience.

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

[39]  M. Häusser,et al.  Propagation of action potentials in dendrites depends on dendritic morphology. , 2001, Journal of neurophysiology.

[40]  H. S. Meyer,et al.  Cell Type–Specific Three-Dimensional Structure of Thalamocortical Circuits in a Column of Rat Vibrissal Cortex , 2011, Cerebral cortex.

[41]  B W Connors,et al.  Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I , 1998, The Journal of comparative neurology.

[42]  W. Senn,et al.  Top-down dendritic input increases the gain of layer 5 pyramidal neurons. , 2004, Cerebral cortex.

[43]  Mark T. Harnett,et al.  Nonlinear dendritic integration of sensory and motor input during an active sensing task , 2012, Nature.

[44]  Alon Korngreen,et al.  Dendritic voltage‐gated K+ conductance gradient in pyramidal neurones of neocortical layer 5B from rats , 2007, The Journal of physiology.

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

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