Dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neurons

A gradient in the density of hyperpolarization-activated cyclic-nucleotide gated (HCN) channels is necessary for the emergence of several functional maps within hippocampal pyramidal neurons. Here, we systematically analyzed the impact of dendritic atrophy on nine such functional maps, related to in...

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Main Authors: Neha eDhupia, Rahul Kumar Rathour, Rishikesh eNarayanan
Format: Article
Language:English
Published: Frontiers Media S.A. 2015-01-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fncel.2014.00456/full
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spelling doaj-bec6dba775a24f72bc2f359136127e4e2020-11-24T23:14:23ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022015-01-01810.3389/fncel.2014.00456118039Dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neuronsNeha eDhupia0Neha eDhupia1Rahul Kumar Rathour2Rishikesh eNarayanan3Indian Institute of ScienceUniversity of RajasthanIndian Institute of ScienceIndian Institute of ScienceA gradient in the density of hyperpolarization-activated cyclic-nucleotide gated (HCN) channels is necessary for the emergence of several functional maps within hippocampal pyramidal neurons. Here, we systematically analyzed the impact of dendritic atrophy on nine such functional maps, related to input resistance and local/transfer impedance properties, using conductance-based models of hippocampal pyramidal neurons. We introduced progressive dendritic atrophy in a CA1 pyramidal neuron reconstruction through a pruning algorithm, measured all functional maps in each pruned reconstruction, and arrived at functional forms for the dependence of underlying measurements on dendritic length. We found that, across frequencies, atrophied neurons responded with higher efficiency to incoming inputs, and the transfer of signals across the dendritic tree was more effective in an atrophied reconstruction. Importantly, despite the presence of identical HCN-channel density gradients, spatial gradients in input resistance, local/transfer resonance frequencies and impedance profiles were significantly constricted in reconstructions with dendritic atrophy, where these physiological measurements across dendritic locations converged to similar values. These results revealed that, in atrophied dendritic structures, the presence of an ion channel density gradient alone was insufficient to sustain homologous functional maps along the same neuronal topograph. We assessed the biophysical basis for these conclusions and found that this atrophy-induced constriction of functional maps was mediated by an enhanced spatial spread of the influence of an HCN-channel cluster in atrophied trees. These results demonstrated that the influence fields of ion channel conductances need to be localized for channel gradients to express themselves as homologous functional maps, suggesting that ion channel gradients are necessary but not sufficient for the emergence of functional maps within single neurons.http://journal.frontiersin.org/Journal/10.3389/fncel.2014.00456/fullresonancedendritic morphologyfunctional mapsimpedanceHCN channel
collection DOAJ
language English
format Article
sources DOAJ
author Neha eDhupia
Neha eDhupia
Rahul Kumar Rathour
Rishikesh eNarayanan
spellingShingle Neha eDhupia
Neha eDhupia
Rahul Kumar Rathour
Rishikesh eNarayanan
Dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neurons
Frontiers in Cellular Neuroscience
resonance
dendritic morphology
functional maps
impedance
HCN channel
author_facet Neha eDhupia
Neha eDhupia
Rahul Kumar Rathour
Rishikesh eNarayanan
author_sort Neha eDhupia
title Dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neurons
title_short Dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neurons
title_full Dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neurons
title_fullStr Dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neurons
title_full_unstemmed Dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neurons
title_sort dendritic atrophy constricts functional maps in resonance and impedance properties of hippocampal model neurons
publisher Frontiers Media S.A.
series Frontiers in Cellular Neuroscience
issn 1662-5102
publishDate 2015-01-01
description A gradient in the density of hyperpolarization-activated cyclic-nucleotide gated (HCN) channels is necessary for the emergence of several functional maps within hippocampal pyramidal neurons. Here, we systematically analyzed the impact of dendritic atrophy on nine such functional maps, related to input resistance and local/transfer impedance properties, using conductance-based models of hippocampal pyramidal neurons. We introduced progressive dendritic atrophy in a CA1 pyramidal neuron reconstruction through a pruning algorithm, measured all functional maps in each pruned reconstruction, and arrived at functional forms for the dependence of underlying measurements on dendritic length. We found that, across frequencies, atrophied neurons responded with higher efficiency to incoming inputs, and the transfer of signals across the dendritic tree was more effective in an atrophied reconstruction. Importantly, despite the presence of identical HCN-channel density gradients, spatial gradients in input resistance, local/transfer resonance frequencies and impedance profiles were significantly constricted in reconstructions with dendritic atrophy, where these physiological measurements across dendritic locations converged to similar values. These results revealed that, in atrophied dendritic structures, the presence of an ion channel density gradient alone was insufficient to sustain homologous functional maps along the same neuronal topograph. We assessed the biophysical basis for these conclusions and found that this atrophy-induced constriction of functional maps was mediated by an enhanced spatial spread of the influence of an HCN-channel cluster in atrophied trees. These results demonstrated that the influence fields of ion channel conductances need to be localized for channel gradients to express themselves as homologous functional maps, suggesting that ion channel gradients are necessary but not sufficient for the emergence of functional maps within single neurons.
topic resonance
dendritic morphology
functional maps
impedance
HCN channel
url http://journal.frontiersin.org/Journal/10.3389/fncel.2014.00456/full
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