Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus

Hippocampal place cells represent nonspatial information through a process called rate remapping, which involves a change in the firing rate of a place cell without changes in its spatial specificity. However, many hippocampal phenomena occur on very short time scales over which long-term average fi...

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Main Authors: Sanders, Honi, Ji, Daoyun, Sasaki, Takuya, Leutgeb, Jill K., Wilson, Matthew A., Lisman, John E.
Other Authors: Picower Institute for Learning and Memory
Format: Article
Language:English
Published: Wiley 2019
Online Access:https://hdl.handle.net/1721.1/122459
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author Sanders, Honi
Ji, Daoyun
Sasaki, Takuya
Leutgeb, Jill K.
Wilson, Matthew A.
Lisman, John E.
author2 Picower Institute for Learning and Memory
author_facet Picower Institute for Learning and Memory
Sanders, Honi
Ji, Daoyun
Sasaki, Takuya
Leutgeb, Jill K.
Wilson, Matthew A.
Lisman, John E.
author_sort Sanders, Honi
collection MIT
description Hippocampal place cells represent nonspatial information through a process called rate remapping, which involves a change in the firing rate of a place cell without changes in its spatial specificity. However, many hippocampal phenomena occur on very short time scales over which long-term average firing rates are not an appropriate description of activity. To understand how rate remapping relates to fine-scale temporal firing phenomena, we asked how rate remapping affected burst firing and trial-to-trial spike count variability. In addition, we looked at how rate remapping relates to the theta-frequency oscillations of the hippocampus, which are thought to temporally organize firing on time scales faster than 100 ms. We found that theta phase coding was preserved through changes in firing rate due to rate remapping. Interestingly, rate remapping in CA1 in response to task demands preferentially occurred during the first half of the theta cycle. The other half of the theta cycle contained preferential expression of phase precession, a phenomenon associated with place cell sequences, in agreement with previous results. This difference of place cell coding during different halves of the theta cycle supports recent theoretical suggestions that different processes occur during the two halves of the theta cycle. The differentiation between the halves of the theta cycle was not clear in recordings from CA3 during rate remapping induced by task-irrelevant sensory changes. These findings provide new insight into the way that temporal coding is utilized in the hippocampus and how rate remapping is expressed through that temporal code. Keywords: overdispersion; phase precession; place cells; theta rhythm; theta sequence
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spelling mit-1721.1/1224592022-09-23T10:18:42Z Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus Sanders, Honi Ji, Daoyun Sasaki, Takuya Leutgeb, Jill K. Wilson, Matthew A. Lisman, John E. Picower Institute for Learning and Memory Hippocampal place cells represent nonspatial information through a process called rate remapping, which involves a change in the firing rate of a place cell without changes in its spatial specificity. However, many hippocampal phenomena occur on very short time scales over which long-term average firing rates are not an appropriate description of activity. To understand how rate remapping relates to fine-scale temporal firing phenomena, we asked how rate remapping affected burst firing and trial-to-trial spike count variability. In addition, we looked at how rate remapping relates to the theta-frequency oscillations of the hippocampus, which are thought to temporally organize firing on time scales faster than 100 ms. We found that theta phase coding was preserved through changes in firing rate due to rate remapping. Interestingly, rate remapping in CA1 in response to task demands preferentially occurred during the first half of the theta cycle. The other half of the theta cycle contained preferential expression of phase precession, a phenomenon associated with place cell sequences, in agreement with previous results. This difference of place cell coding during different halves of the theta cycle supports recent theoretical suggestions that different processes occur during the two halves of the theta cycle. The differentiation between the halves of the theta cycle was not clear in recordings from CA3 during rate remapping induced by task-irrelevant sensory changes. These findings provide new insight into the way that temporal coding is utilized in the hippocampus and how rate remapping is expressed through that temporal code. Keywords: overdispersion; phase precession; place cells; theta rhythm; theta sequence National Science Foundation (U.S.) (Grant 1R01DA027807) National Science Foundation (U.S.) (Grant DGE‐1068620) National Institute of Mental Health (U.S.) (Grant R01MH061976) National Institute of Mental Health (U.S.) (Grant R01MH100349) National Institute of Mental Health (U.S.) (Grant R01MH102841) National Institute of Mental Health (U.S.) (Grant F31MH103966) 2019-10-07T20:33:42Z 2019-10-07T20:33:42Z 2018-11 2018-07 2019-10-04T18:21:58Z Article http://purl.org/eprint/type/JournalArticle 1050-9631 https://hdl.handle.net/1721.1/122459 Sanders, Honi et al. "Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus." Hippocampus 29, 2 (November 2018) © 2018 Wiley Periodicals, Inc en http://dx.doi.org/10.1002/hipo.23020 Hippocampus Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/4.0/ application/pdf Wiley Other repository
spellingShingle Sanders, Honi
Ji, Daoyun
Sasaki, Takuya
Leutgeb, Jill K.
Wilson, Matthew A.
Lisman, John E.
Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus
title Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus
title_full Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus
title_fullStr Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus
title_full_unstemmed Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus
title_short Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus
title_sort temporal coding and rate remapping representation of nonspatial information in the hippocampus
url https://hdl.handle.net/1721.1/122459
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