Literature DB >> 33689489

Effects of Ih and TASK-like shunting current on dendritic impedance in layer 5 pyramidal-tract neurons.

Craig Kelley1, Salvador Dura-Bernal2,3, Samuel A Neymotin3,4, Srdjan D Antic5, Nicholas T Carnevale6, Michele Migliore7, William W Lytton1,2,8,9,10.   

Abstract

Pyramidal neurons in neocortex have complex input-output relationships that depend on their morphologies, ion channel distributions, and the nature of their inputs, but which cannot be replicated by simple integrate-and-fire models. The impedance properties of their dendritic arbors, such as resonance and phase shift, shape neuronal responses to synaptic inputs and provide intraneuronal functional maps reflecting their intrinsic dynamics and excitability. Experimental studies of dendritic impedance have shown that neocortical pyramidal tract neurons exhibit distance-dependent changes in resonance and impedance phase with respect to the soma. We, therefore, investigated how well several biophysically detailed multicompartment models of neocortical layer 5 pyramidal tract neurons reproduce the location-dependent impedance profiles observed experimentally. Each model tested here exhibited location-dependent impedance profiles, but most captured either the observed impedance amplitude or phase, not both. The only model that captured features from both incorporates hyperpolarization-activated cyclic nucleotide-gated (HCN) channels and a shunting current, such as that produced by Twik-related acid-sensitive K+ (TASK) channels. TASK-like channel density in this model was proportional to local HCN channel density. We found that although this shunting current alone is insufficient to produce resonance or realistic phase response, it modulates all features of dendritic impedance, including resonance frequencies, resonance strength, synchronous frequencies, and total inductive phase. We also explored how the interaction of HCN channel current (Ih) and a TASK-like shunting current shape synaptic potentials and produce degeneracy in dendritic impedance profiles, wherein different combinations of Ih and shunting current can produce the same impedance profile.NEW & NOTEWORTHY We simulated chirp current stimulation in the apical dendrites of 5 biophysically detailed multicompartment models of neocortical pyramidal tract neurons and found that a combination of HCN channels and TASK-like channels produced the best fit to experimental measurements of dendritic impedance. We then explored how HCN and TASK-like channels can shape the dendritic impedance as well as the voltage response to synaptic currents.

Entities:  

Keywords:  Twik-related acid-sensitive K+(TASK) channels; h-current (Ih); impedance; pyramidal tract neurons; resonance

Mesh:

Substances:

Year:  2021        PMID: 33689489      PMCID: PMC8282219          DOI: 10.1152/jn.00015.2021

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  88 in total

Review 1.  Hyperpolarization-activated cation currents: from molecules to physiological function.

Authors:  Richard B Robinson; Steven A Siegelbaum
Journal:  Annu Rev Physiol       Date:  2002-11-19       Impact factor: 19.318

2.  Dendrite-to-soma input/output function of continuous time-varying signals in hippocampal CA1 pyramidal neurons.

Authors:  Erik P Cook; Jennifer A Guest; Yong Liang; Nicolas Y Masse; Costa M Colbert
Journal:  J Neurophysiol       Date:  2007-09-19       Impact factor: 2.714

3.  Some physical aspects of bioelectric phenomena.

Authors:  K S COLE
Journal:  Proc Natl Acad Sci U S A       Date:  1949-10       Impact factor: 11.205

4.  Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea.

Authors:  Eunyoung Yi; Isabelle Roux; Elisabeth Glowatzki
Journal:  J Neurophysiol       Date:  2010-03-10       Impact factor: 2.714

5.  Primary involvement of K+ conductance in membrane resonance of trigeminal root ganglion neurons.

Authors:  E Puil; B Gimbarzevsky; I Spigelman
Journal:  J Neurophysiol       Date:  1988-01       Impact factor: 2.714

6.  Subthreshold behavior and phenomenological impedance of the squid giant axon.

Authors:  A Mauro; F Conti; F Dodge; R Schor
Journal:  J Gen Physiol       Date:  1970-04       Impact factor: 4.086

7.  Adrenergic Modulation Regulates the Dendritic Excitability of Layer 5 Pyramidal Neurons In Vivo.

Authors:  Christina Labarrera; Yair Deitcher; Amir Dudai; Benjamin Weiner; Adi Kaduri Amichai; Neta Zylbermann; Michael London
Journal:  Cell Rep       Date:  2018-04-24       Impact factor: 9.423

8.  Cell type-specific thalamic innervation in a column of rat vibrissal cortex.

Authors:  Hanno S Meyer; Verena C Wimmer; Mike Hemberger; Randy M Bruno; Christiaan P J de Kock; Andreas Frick; Bert Sakmann; Moritz Helmstaedter
Journal:  Cereb Cortex       Date:  2010-06-09       Impact factor: 5.357

9.  h channel-dependent deficit of theta oscillation resonance and phase shift in temporal lobe epilepsy.

Authors:  Béatrice Marcelin; Laëtitia Chauvière; Albert Becker; Michele Migliore; Monique Esclapez; Christophe Bernard
Journal:  Neurobiol Dis       Date:  2008-12-16       Impact factor: 5.996

Review 10.  Dendritic ion channel trafficking and plasticity.

Authors:  Mala M Shah; Rebecca S Hammond; Dax A Hoffman
Journal:  Trends Neurosci       Date:  2010-04-01       Impact factor: 13.837

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  3 in total

1.  Excitatory and inhibitory effects of HCN channel modulation on excitability of layer V pyramidal cells.

Authors:  Tuomo Mäki-Marttunen; Verónica Mäki-Marttunen
Journal:  PLoS Comput Biol       Date:  2022-09-13       Impact factor: 4.779

2.  Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex.

Authors:  Samuel A Neymotin; Idan Tal; Annamaria Barczak; Monica N O'Connell; Tammy McGinnis; Noah Markowitz; Elizabeth Espinal; Erica Griffith; Haroon Anwar; Salvador Dura-Bernal; Charles E Schroeder; William W Lytton; Stephanie R Jones; Stephan Bickel; Peter Lakatos
Journal:  eNeuro       Date:  2022-08-19

3.  Ion-channel degeneracy: Multiple ion channels heterogeneously regulate intrinsic physiology of rat hippocampal granule cells.

Authors:  Poonam Mishra; Rishikesh Narayanan
Journal:  Physiol Rep       Date:  2021-08
  3 in total

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