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Research ArticleNew Research, Disorders of the Nervous System

Cortico-Striatal Cross-Frequency Coupling and Gamma Genesis Disruptions in Huntington’s Disease Mouse and Computational Models

Sebastien Naze, James Humble, Pengsheng Zheng, Scott Barton, Claudia Rangel-Barajas, George V. Rebec and James R. Kozloski
eNeuro 29 November 2018, 5 (6) ENEURO.0210-18.2018; DOI: https://doi.org/10.1523/ENEURO.0210-18.2018
Sebastien Naze
1 T.J. Watson IBM Research Center, Yorktown Heights, NY 10598
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James Humble
1 T.J. Watson IBM Research Center, Yorktown Heights, NY 10598
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Pengsheng Zheng
1 T.J. Watson IBM Research Center, Yorktown Heights, NY 10598
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Scott Barton
2Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN 47405
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Claudia Rangel-Barajas
2Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN 47405
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George V. Rebec
2Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN 47405
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James R. Kozloski
1 T.J. Watson IBM Research Center, Yorktown Heights, NY 10598
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Abstract

Abnormal gamma band power across cortex and striatum is an important phenotype of Huntington’s disease (HD) in both patients and animal models, but neither the origin nor the functional relevance of this phenotype is well understood. Here, we analyzed local field potential (LFP) activity in freely behaving, symptomatic R6/2 and Q175 mouse models and corresponding wild-type (WT) controls. We focused on periods of quiet rest, which show strong γ activity in HD mice. Simultaneous recording from motor cortex and its target area in dorsal striatum in the R6/2 model revealed exaggerated functional coupling over that observed in WT between the phase of delta frequencies (1–4 Hz) in cortex and striatum and striatal amplitude modulation of low γ frequencies (25–55 Hz; i.e., phase-amplitude coupling, PAC), but no evidence that abnormal cortical activity alone can account for the increase in striatal γ power. Both HD mouse models had stronger coupling of γ amplitude to δ phase and more unimodal phase distributions than their WT counterparts. To assess the possible role of striatal fast-spiking interneurons (FSIs) in these phenomena, we developed a computational model based on additional striatal recordings from Q175 mice. Changes in peak γ frequency and power ratio were readily reproduced by our computational model, accounting for several experimental findings reported in the literature. Our results suggest that HD is characterized by both a reorganization of cortico-striatal drive and specific population changes related to intrastriatal synaptic coupling.

  • fast-spiking interneuron
  • gamma
  • Huntington’s disease

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported partly by the CHDI Foundation.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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eneuro: 5 (6)
eNeuro
Vol. 5, Issue 6
November/December 2018
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Cortico-Striatal Cross-Frequency Coupling and Gamma Genesis Disruptions in Huntington’s Disease Mouse and Computational Models
Sebastien Naze, James Humble, Pengsheng Zheng, Scott Barton, Claudia Rangel-Barajas, George V. Rebec, James R. Kozloski
eNeuro 29 November 2018, 5 (6) ENEURO.0210-18.2018; DOI: 10.1523/ENEURO.0210-18.2018

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Cortico-Striatal Cross-Frequency Coupling and Gamma Genesis Disruptions in Huntington’s Disease Mouse and Computational Models
Sebastien Naze, James Humble, Pengsheng Zheng, Scott Barton, Claudia Rangel-Barajas, George V. Rebec, James R. Kozloski
eNeuro 29 November 2018, 5 (6) ENEURO.0210-18.2018; DOI: 10.1523/ENEURO.0210-18.2018
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Keywords

  • fast-spiking interneuron
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