Control of recollection by slow gamma dominating mid-frequency gamma in hippocampus CA1

Dino Dvorak; Basma Radwan; Fraser T. Sparks; Zoe Nicole Talbot; André A. Fenton

doi:10.1371/journal.pbio.2003354

Control of recollection by slow gamma dominating mid-frequency gamma in hippocampus CA1

Dino Dvorak, Basma Radwan, Fraser T. Sparks, Zoe Nicole Talbot, André A. Fenton

Neural Science

Research output: Contribution to journal › Article › peer-review

Abstract

Behavior is used to assess memory and cognitive deficits in animals like Fmr1-null mice that model Fragile X Syndrome, but behavior is a proxy for unknown neural events that define cognitive variables like recollection. We identified an electrophysiological signature of recollection in mouse dorsal Cornu Ammonis 1 (CA1) hippocampus. During a shocked-place avoidance task, slow gamma (SG) (30–50 Hz) dominates mid-frequency gamma (MG) (70–90 Hz) oscillations 2–3 s before successful avoidance, but not failures. Wild-type (WT) but not Fmr1-null mice rapidly adapt to relocating the shock; concurrently, SG/MG maxima (SG_dom) decrease in WT but not in cognitively inflexible Fmr1-null mice. During SG_dom, putative pyramidal cell ensembles represent distant locations; during place avoidance, these are avoided places. During shock relocation, WT ensembles represent distant locations near the currently correct shock zone, but Fmr1-null ensembles represent the formerly correct zone. These findings indicate that recollection occurs when CA1 SG dominates MG and that accurate recollection of inappropriate memories explains Fmr1-null cognitive inflexibility.

Original language	English (US)
Article number	e2003354
Journal	PLoS biology
Volume	16
Issue number	1
DOIs	https://doi.org/10.1371/journal.pbio.2003354
State	Published - Jan 2018

ASJC Scopus subject areas

Neuroscience(all)
Biochemistry, Genetics and Molecular Biology(all)
Immunology and Microbiology(all)
Agricultural and Biological Sciences(all)

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10.1371/journal.pbio.2003354

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title = "Control of recollection by slow gamma dominating mid-frequency gamma in hippocampus CA1",

abstract = "Behavior is used to assess memory and cognitive deficits in animals like Fmr1-null mice that model Fragile X Syndrome, but behavior is a proxy for unknown neural events that define cognitive variables like recollection. We identified an electrophysiological signature of recollection in mouse dorsal Cornu Ammonis 1 (CA1) hippocampus. During a shocked-place avoidance task, slow gamma (SG) (30–50 Hz) dominates mid-frequency gamma (MG) (70–90 Hz) oscillations 2–3 s before successful avoidance, but not failures. Wild-type (WT) but not Fmr1-null mice rapidly adapt to relocating the shock; concurrently, SG/MG maxima (SGdom) decrease in WT but not in cognitively inflexible Fmr1-null mice. During SGdom, putative pyramidal cell ensembles represent distant locations; during place avoidance, these are avoided places. During shock relocation, WT ensembles represent distant locations near the currently correct shock zone, but Fmr1-null ensembles represent the formerly correct zone. These findings indicate that recollection occurs when CA1 SG dominates MG and that accurate recollection of inappropriate memories explains Fmr1-null cognitive inflexibility.",

author = "Dino Dvorak and Basma Radwan and Sparks, {Fraser T.} and Talbot, {Zoe Nicole} and Fenton, {Andr{\'e} A.}",

note = "Funding Information: Canadian Institutes of Health Research http://www.cihr-irsc.gc.ca/ (grant number 201411MFE-339265-171319). Received by FTS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Institute of Health https://www.nih.gov/ (grant number RO1MH099128). Received by AAF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Simons Foundation https://www.simonsfoundation.org/ (grant number 294388). Received by AAF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: {\textcopyright} 2018 Dvorak et al.",

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AU - Talbot, Zoe Nicole

AU - Fenton, André A.

N1 - Funding Information: Canadian Institutes of Health Research http://www.cihr-irsc.gc.ca/ (grant number 201411MFE-339265-171319). Received by FTS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Institute of Health https://www.nih.gov/ (grant number RO1MH099128). Received by AAF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Simons Foundation https://www.simonsfoundation.org/ (grant number 294388). Received by AAF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: © 2018 Dvorak et al.

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N2 - Behavior is used to assess memory and cognitive deficits in animals like Fmr1-null mice that model Fragile X Syndrome, but behavior is a proxy for unknown neural events that define cognitive variables like recollection. We identified an electrophysiological signature of recollection in mouse dorsal Cornu Ammonis 1 (CA1) hippocampus. During a shocked-place avoidance task, slow gamma (SG) (30–50 Hz) dominates mid-frequency gamma (MG) (70–90 Hz) oscillations 2–3 s before successful avoidance, but not failures. Wild-type (WT) but not Fmr1-null mice rapidly adapt to relocating the shock; concurrently, SG/MG maxima (SGdom) decrease in WT but not in cognitively inflexible Fmr1-null mice. During SGdom, putative pyramidal cell ensembles represent distant locations; during place avoidance, these are avoided places. During shock relocation, WT ensembles represent distant locations near the currently correct shock zone, but Fmr1-null ensembles represent the formerly correct zone. These findings indicate that recollection occurs when CA1 SG dominates MG and that accurate recollection of inappropriate memories explains Fmr1-null cognitive inflexibility.

AB - Behavior is used to assess memory and cognitive deficits in animals like Fmr1-null mice that model Fragile X Syndrome, but behavior is a proxy for unknown neural events that define cognitive variables like recollection. We identified an electrophysiological signature of recollection in mouse dorsal Cornu Ammonis 1 (CA1) hippocampus. During a shocked-place avoidance task, slow gamma (SG) (30–50 Hz) dominates mid-frequency gamma (MG) (70–90 Hz) oscillations 2–3 s before successful avoidance, but not failures. Wild-type (WT) but not Fmr1-null mice rapidly adapt to relocating the shock; concurrently, SG/MG maxima (SGdom) decrease in WT but not in cognitively inflexible Fmr1-null mice. During SGdom, putative pyramidal cell ensembles represent distant locations; during place avoidance, these are avoided places. During shock relocation, WT ensembles represent distant locations near the currently correct shock zone, but Fmr1-null ensembles represent the formerly correct zone. These findings indicate that recollection occurs when CA1 SG dominates MG and that accurate recollection of inappropriate memories explains Fmr1-null cognitive inflexibility.

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Control of recollection by slow gamma dominating mid-frequency gamma in hippocampus CA1

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