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Broadband Entrainment of Striatal Low-Threshold Spike Interneurons

Striatal interneurons and spiny projection (SP) neurons are differentially tuned to spectral components of their input. Previous studies showed that spike responses of somatostatin/NPY-expressing low threshold spike (LTS) interneurons have broad frequency tuning, setting these cells apart from other...

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Autores principales: Morales, Juan C., Higgs, Matthew H., Song, Soomin C., Wilson, Charles J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7326000/
https://www.ncbi.nlm.nih.gov/pubmed/32655378
http://dx.doi.org/10.3389/fncir.2020.00036
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author Morales, Juan C.
Higgs, Matthew H.
Song, Soomin C.
Wilson, Charles J.
author_facet Morales, Juan C.
Higgs, Matthew H.
Song, Soomin C.
Wilson, Charles J.
author_sort Morales, Juan C.
collection PubMed
description Striatal interneurons and spiny projection (SP) neurons are differentially tuned to spectral components of their input. Previous studies showed that spike responses of somatostatin/NPY-expressing low threshold spike (LTS) interneurons have broad frequency tuning, setting these cells apart from other striatal GABAergic interneurons and SP neurons. We investigated the mechanism of LTS interneuron spiking resonance and its relationship to non-spiking membrane impedance resonance, finding that abolition of impedance resonance did not alter spiking resonance. Because LTS interneurons are pacemakers whose rhythmic firing is perturbed by synaptic input, we tested the hypothesis that their spiking resonance arises from their phase resetting properties. Phase resetting curves (PRCs) were measured in LTS interneurons and SP neurons and used to make phase-oscillator models of both cell types. The models reproduced the broad tuning of LTS interneurons, and the differences from SP neurons. The spectral components of the PRC predicted each cell’s sensitivity to corresponding input frequencies. LTS interneuron PRCs contain larger high-frequency components than SP neuron PRCs, providing enhanced responses to input frequencies above the cells’ average firing rates. Thus, LTS cells can be entrained by input oscillations to which SP neurons are less responsive. These findings suggest that feedforward inhibition by LTS interneurons may regulate SP neurons’ entrainment by oscillatory afferents.
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spelling pubmed-73260002020-07-09 Broadband Entrainment of Striatal Low-Threshold Spike Interneurons Morales, Juan C. Higgs, Matthew H. Song, Soomin C. Wilson, Charles J. Front Neural Circuits Neuroscience Striatal interneurons and spiny projection (SP) neurons are differentially tuned to spectral components of their input. Previous studies showed that spike responses of somatostatin/NPY-expressing low threshold spike (LTS) interneurons have broad frequency tuning, setting these cells apart from other striatal GABAergic interneurons and SP neurons. We investigated the mechanism of LTS interneuron spiking resonance and its relationship to non-spiking membrane impedance resonance, finding that abolition of impedance resonance did not alter spiking resonance. Because LTS interneurons are pacemakers whose rhythmic firing is perturbed by synaptic input, we tested the hypothesis that their spiking resonance arises from their phase resetting properties. Phase resetting curves (PRCs) were measured in LTS interneurons and SP neurons and used to make phase-oscillator models of both cell types. The models reproduced the broad tuning of LTS interneurons, and the differences from SP neurons. The spectral components of the PRC predicted each cell’s sensitivity to corresponding input frequencies. LTS interneuron PRCs contain larger high-frequency components than SP neuron PRCs, providing enhanced responses to input frequencies above the cells’ average firing rates. Thus, LTS cells can be entrained by input oscillations to which SP neurons are less responsive. These findings suggest that feedforward inhibition by LTS interneurons may regulate SP neurons’ entrainment by oscillatory afferents. Frontiers Media S.A. 2020-06-12 /pmc/articles/PMC7326000/ /pubmed/32655378 http://dx.doi.org/10.3389/fncir.2020.00036 Text en Copyright © 2020 Morales, Higgs, Song and Wilson. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Morales, Juan C.
Higgs, Matthew H.
Song, Soomin C.
Wilson, Charles J.
Broadband Entrainment of Striatal Low-Threshold Spike Interneurons
title Broadband Entrainment of Striatal Low-Threshold Spike Interneurons
title_full Broadband Entrainment of Striatal Low-Threshold Spike Interneurons
title_fullStr Broadband Entrainment of Striatal Low-Threshold Spike Interneurons
title_full_unstemmed Broadband Entrainment of Striatal Low-Threshold Spike Interneurons
title_short Broadband Entrainment of Striatal Low-Threshold Spike Interneurons
title_sort broadband entrainment of striatal low-threshold spike interneurons
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7326000/
https://www.ncbi.nlm.nih.gov/pubmed/32655378
http://dx.doi.org/10.3389/fncir.2020.00036
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