Loading…

Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus

A key question in the analysis of hippocampal memory relates to how attention modulates the encoding and long-term retrieval of spatial and nonspatial representations in this region. To address this question, we recorded from single cells over a period of 5 days in the CA1 region of the dorsal hippo...

Full description

Saved in:
Bibliographic Details
Published in:PLoS biology 2009-06, Vol.7 (6), p.e1000140-e1000140
Main Authors: Muzzio, Isabel A, Levita, Liat, Kulkarni, Jayant, Monaco, Joseph, Kentros, Clifford, Stead, Matthew, Abbott, Larry F, Kandel, Eric R
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c665t-a197934290d44d3e5da7b5321f060af142d478162629d385769dbfd0fbe8b5563
cites cdi_FETCH-LOGICAL-c665t-a197934290d44d3e5da7b5321f060af142d478162629d385769dbfd0fbe8b5563
container_end_page e1000140
container_issue 6
container_start_page e1000140
container_title PLoS biology
container_volume 7
creator Muzzio, Isabel A
Levita, Liat
Kulkarni, Jayant
Monaco, Joseph
Kentros, Clifford
Stead, Matthew
Abbott, Larry F
Kandel, Eric R
description A key question in the analysis of hippocampal memory relates to how attention modulates the encoding and long-term retrieval of spatial and nonspatial representations in this region. To address this question, we recorded from single cells over a period of 5 days in the CA1 region of the dorsal hippocampus while mice acquired one of two goal-oriented tasks. These tasks required the animals to find a hidden food reward by attending to either the visuospatial environment or a particular odor presented in shifting spatial locations. Attention to the visuospatial environment increased the stability of visuospatial representations and phase locking to gamma oscillations--a form of neuronal synchronization thought to underlie the attentional mechanism necessary for processing task-relevant information. Attention to a spatially shifting olfactory cue compromised the stability of place fields and increased the stability of reward-associated odor representations, which were most consistently retrieved during periods of sniffing and digging when animals were restricted to the cup locations. Together, these results suggest that attention selectively modulates the encoding and retrieval of hippocampal representations by enhancing physiological responses to task-relevant information.
doi_str_mv 10.1371/journal.pbio.1000140
format article
fullrecord <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_1297521918</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A638106067</galeid><doaj_id>oai_doaj_org_article_bf4243c096be4c6cbbc9e6e76ed26e83</doaj_id><sourcerecordid>A638106067</sourcerecordid><originalsourceid>FETCH-LOGICAL-c665t-a197934290d44d3e5da7b5321f060af142d478162629d385769dbfd0fbe8b5563</originalsourceid><addsrcrecordid>eNqVkluL1DAYhoso7rr6D0QLguDFjDk1bW6EYfEwsLjg6TakydeZLJ2kJung_HvTnao74IXSi5bkeZ-0b7-ieIrREtMav77xY3CqXw6t9UuMEMIM3SvOccWqRd001f07z2fFoxhvECJEkOZhcYZFxZlA9LzYr1ICl6x3JbitchpimbZQBkjBwl71pXKmjEm1trfpUPqu3Ns4-jioZOdd33dKJx8OOTUEiNmnJmMsrbuVGR9iZrd2GLxWu2GMj4sHneojPJnvF8XXd2-_XH5YXF2_X1-urhaa8yotFBa1oIwIZBgzFCqj6raiBHeII9VhRgyrG8wJJ8LQpqq5MG1nUNdC01YVpxfF86N36H2Uc2VRYiLqimCBm0ysj4Tx6kYOwe5UOEivrLxd8GEjVUhW9yDbjhFGNRK8Baa5blstgEPNwRAODc2uN_NpY7sDo3MRQfUn0tMdZ7dy4_eScMEpq7Pg5SwI_vsIMcmdjRr6XjnwY5S8ZhQJOn3XiyO4UfnFrOt89ukJlitOG5zr4ZNu-RcqXwZ2VnsHnc3rJ4FXJ4HMJPiRNmqMUa4_f_oP9uO_s9ffTll2ZHXwMQbofveHkZwm_9dvlNPky3nyc-zZ3e7_hOZRpz8BQOIBQQ</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>67430936</pqid></control><display><type>article</type><title>Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus</title><source>Publicly Available Content Database (Proquest) (PQ_SDU_P3)</source><source>PubMed Central</source><creator>Muzzio, Isabel A ; Levita, Liat ; Kulkarni, Jayant ; Monaco, Joseph ; Kentros, Clifford ; Stead, Matthew ; Abbott, Larry F ; Kandel, Eric R</creator><contributor>Ungerleider, Leslie</contributor><creatorcontrib>Muzzio, Isabel A ; Levita, Liat ; Kulkarni, Jayant ; Monaco, Joseph ; Kentros, Clifford ; Stead, Matthew ; Abbott, Larry F ; Kandel, Eric R ; Ungerleider, Leslie</creatorcontrib><description>A key question in the analysis of hippocampal memory relates to how attention modulates the encoding and long-term retrieval of spatial and nonspatial representations in this region. To address this question, we recorded from single cells over a period of 5 days in the CA1 region of the dorsal hippocampus while mice acquired one of two goal-oriented tasks. These tasks required the animals to find a hidden food reward by attending to either the visuospatial environment or a particular odor presented in shifting spatial locations. Attention to the visuospatial environment increased the stability of visuospatial representations and phase locking to gamma oscillations--a form of neuronal synchronization thought to underlie the attentional mechanism necessary for processing task-relevant information. Attention to a spatially shifting olfactory cue compromised the stability of place fields and increased the stability of reward-associated odor representations, which were most consistently retrieved during periods of sniffing and digging when animals were restricted to the cup locations. Together, these results suggest that attention selectively modulates the encoding and retrieval of hippocampal representations by enhancing physiological responses to task-relevant information.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.1000140</identifier><identifier>PMID: 19564903</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Action Potentials - physiology ; Analysis ; Animals ; Attention ; Attention - physiology ; Controlled processes (Cognition) ; Cues ; Goals ; Hippocampus (Brain) ; Hippocampus - cytology ; Hippocampus - physiology ; Male ; Memory ; Mice ; Mice, Inbred C57BL ; Models, Neurological ; Neuroscience ; Neuroscience/Animal Cognition ; Neuroscience/Behavioral Neuroscience ; Neuroscience/Cognitive Neuroscience ; Observations ; Odorants ; Odors ; Olfactory Pathways - physiology ; Physiological aspects ; Psychomotor Performance ; Pyramidal Cells - cytology ; Pyramidal Cells - physiology ; Reaction Time - physiology ; Reward ; Rodents ; Smell ; Spatial Behavior - physiology ; Spatial behavior in animals ; Studies ; Visual Perception - physiology</subject><ispartof>PLoS biology, 2009-06, Vol.7 (6), p.e1000140-e1000140</ispartof><rights>COPYRIGHT 2009 Public Library of Science</rights><rights>Muzzio et al. 2009</rights><rights>2009 Muzzio et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Muzzio IA, Levita L, Kulkarni J, Monaco J, Kentros C, et al. (2009) Attention Enhances the Retrieval and Stability of Visuospatial and Olfactory Representations in the Dorsal Hippocampus. PLoS Biol 7(6): e1000140. doi:10.1371/journal.pbio.1000140</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c665t-a197934290d44d3e5da7b5321f060af142d478162629d385769dbfd0fbe8b5563</citedby><cites>FETCH-LOGICAL-c665t-a197934290d44d3e5da7b5321f060af142d478162629d385769dbfd0fbe8b5563</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2696347/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2696347/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,37013,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19564903$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ungerleider, Leslie</contributor><creatorcontrib>Muzzio, Isabel A</creatorcontrib><creatorcontrib>Levita, Liat</creatorcontrib><creatorcontrib>Kulkarni, Jayant</creatorcontrib><creatorcontrib>Monaco, Joseph</creatorcontrib><creatorcontrib>Kentros, Clifford</creatorcontrib><creatorcontrib>Stead, Matthew</creatorcontrib><creatorcontrib>Abbott, Larry F</creatorcontrib><creatorcontrib>Kandel, Eric R</creatorcontrib><title>Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>A key question in the analysis of hippocampal memory relates to how attention modulates the encoding and long-term retrieval of spatial and nonspatial representations in this region. To address this question, we recorded from single cells over a period of 5 days in the CA1 region of the dorsal hippocampus while mice acquired one of two goal-oriented tasks. These tasks required the animals to find a hidden food reward by attending to either the visuospatial environment or a particular odor presented in shifting spatial locations. Attention to the visuospatial environment increased the stability of visuospatial representations and phase locking to gamma oscillations--a form of neuronal synchronization thought to underlie the attentional mechanism necessary for processing task-relevant information. Attention to a spatially shifting olfactory cue compromised the stability of place fields and increased the stability of reward-associated odor representations, which were most consistently retrieved during periods of sniffing and digging when animals were restricted to the cup locations. Together, these results suggest that attention selectively modulates the encoding and retrieval of hippocampal representations by enhancing physiological responses to task-relevant information.</description><subject>Action Potentials - physiology</subject><subject>Analysis</subject><subject>Animals</subject><subject>Attention</subject><subject>Attention - physiology</subject><subject>Controlled processes (Cognition)</subject><subject>Cues</subject><subject>Goals</subject><subject>Hippocampus (Brain)</subject><subject>Hippocampus - cytology</subject><subject>Hippocampus - physiology</subject><subject>Male</subject><subject>Memory</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Models, Neurological</subject><subject>Neuroscience</subject><subject>Neuroscience/Animal Cognition</subject><subject>Neuroscience/Behavioral Neuroscience</subject><subject>Neuroscience/Cognitive Neuroscience</subject><subject>Observations</subject><subject>Odorants</subject><subject>Odors</subject><subject>Olfactory Pathways - physiology</subject><subject>Physiological aspects</subject><subject>Psychomotor Performance</subject><subject>Pyramidal Cells - cytology</subject><subject>Pyramidal Cells - physiology</subject><subject>Reaction Time - physiology</subject><subject>Reward</subject><subject>Rodents</subject><subject>Smell</subject><subject>Spatial Behavior - physiology</subject><subject>Spatial behavior in animals</subject><subject>Studies</subject><subject>Visual Perception - physiology</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNqVkluL1DAYhoso7rr6D0QLguDFjDk1bW6EYfEwsLjg6TakydeZLJ2kJung_HvTnao74IXSi5bkeZ-0b7-ieIrREtMav77xY3CqXw6t9UuMEMIM3SvOccWqRd001f07z2fFoxhvECJEkOZhcYZFxZlA9LzYr1ICl6x3JbitchpimbZQBkjBwl71pXKmjEm1trfpUPqu3Ns4-jioZOdd33dKJx8OOTUEiNmnJmMsrbuVGR9iZrd2GLxWu2GMj4sHneojPJnvF8XXd2-_XH5YXF2_X1-urhaa8yotFBa1oIwIZBgzFCqj6raiBHeII9VhRgyrG8wJJ8LQpqq5MG1nUNdC01YVpxfF86N36H2Uc2VRYiLqimCBm0ysj4Tx6kYOwe5UOEivrLxd8GEjVUhW9yDbjhFGNRK8Baa5blstgEPNwRAODc2uN_NpY7sDo3MRQfUn0tMdZ7dy4_eScMEpq7Pg5SwI_vsIMcmdjRr6XjnwY5S8ZhQJOn3XiyO4UfnFrOt89ukJlitOG5zr4ZNu-RcqXwZ2VnsHnc3rJ4FXJ4HMJPiRNmqMUa4_f_oP9uO_s9ffTll2ZHXwMQbofveHkZwm_9dvlNPky3nyc-zZ3e7_hOZRpz8BQOIBQQ</recordid><startdate>20090630</startdate><enddate>20090630</enddate><creator>Muzzio, Isabel A</creator><creator>Levita, Liat</creator><creator>Kulkarni, Jayant</creator><creator>Monaco, Joseph</creator><creator>Kentros, Clifford</creator><creator>Stead, Matthew</creator><creator>Abbott, Larry F</creator><creator>Kandel, Eric R</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><scope>CZG</scope></search><sort><creationdate>20090630</creationdate><title>Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus</title><author>Muzzio, Isabel A ; Levita, Liat ; Kulkarni, Jayant ; Monaco, Joseph ; Kentros, Clifford ; Stead, Matthew ; Abbott, Larry F ; Kandel, Eric R</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c665t-a197934290d44d3e5da7b5321f060af142d478162629d385769dbfd0fbe8b5563</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Action Potentials - physiology</topic><topic>Analysis</topic><topic>Animals</topic><topic>Attention</topic><topic>Attention - physiology</topic><topic>Controlled processes (Cognition)</topic><topic>Cues</topic><topic>Goals</topic><topic>Hippocampus (Brain)</topic><topic>Hippocampus - cytology</topic><topic>Hippocampus - physiology</topic><topic>Male</topic><topic>Memory</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Models, Neurological</topic><topic>Neuroscience</topic><topic>Neuroscience/Animal Cognition</topic><topic>Neuroscience/Behavioral Neuroscience</topic><topic>Neuroscience/Cognitive Neuroscience</topic><topic>Observations</topic><topic>Odorants</topic><topic>Odors</topic><topic>Olfactory Pathways - physiology</topic><topic>Physiological aspects</topic><topic>Psychomotor Performance</topic><topic>Pyramidal Cells - cytology</topic><topic>Pyramidal Cells - physiology</topic><topic>Reaction Time - physiology</topic><topic>Reward</topic><topic>Rodents</topic><topic>Smell</topic><topic>Spatial Behavior - physiology</topic><topic>Spatial behavior in animals</topic><topic>Studies</topic><topic>Visual Perception - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Muzzio, Isabel A</creatorcontrib><creatorcontrib>Levita, Liat</creatorcontrib><creatorcontrib>Kulkarni, Jayant</creatorcontrib><creatorcontrib>Monaco, Joseph</creatorcontrib><creatorcontrib>Kentros, Clifford</creatorcontrib><creatorcontrib>Stead, Matthew</creatorcontrib><creatorcontrib>Abbott, Larry F</creatorcontrib><creatorcontrib>Kandel, Eric R</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Muzzio, Isabel A</au><au>Levita, Liat</au><au>Kulkarni, Jayant</au><au>Monaco, Joseph</au><au>Kentros, Clifford</au><au>Stead, Matthew</au><au>Abbott, Larry F</au><au>Kandel, Eric R</au><au>Ungerleider, Leslie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2009-06-30</date><risdate>2009</risdate><volume>7</volume><issue>6</issue><spage>e1000140</spage><epage>e1000140</epage><pages>e1000140-e1000140</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>A key question in the analysis of hippocampal memory relates to how attention modulates the encoding and long-term retrieval of spatial and nonspatial representations in this region. To address this question, we recorded from single cells over a period of 5 days in the CA1 region of the dorsal hippocampus while mice acquired one of two goal-oriented tasks. These tasks required the animals to find a hidden food reward by attending to either the visuospatial environment or a particular odor presented in shifting spatial locations. Attention to the visuospatial environment increased the stability of visuospatial representations and phase locking to gamma oscillations--a form of neuronal synchronization thought to underlie the attentional mechanism necessary for processing task-relevant information. Attention to a spatially shifting olfactory cue compromised the stability of place fields and increased the stability of reward-associated odor representations, which were most consistently retrieved during periods of sniffing and digging when animals were restricted to the cup locations. Together, these results suggest that attention selectively modulates the encoding and retrieval of hippocampal representations by enhancing physiological responses to task-relevant information.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>19564903</pmid><doi>10.1371/journal.pbio.1000140</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1545-7885
ispartof PLoS biology, 2009-06, Vol.7 (6), p.e1000140-e1000140
issn 1545-7885
1544-9173
1545-7885
language eng
recordid cdi_plos_journals_1297521918
source Publicly Available Content Database (Proquest) (PQ_SDU_P3); PubMed Central
subjects Action Potentials - physiology
Analysis
Animals
Attention
Attention - physiology
Controlled processes (Cognition)
Cues
Goals
Hippocampus (Brain)
Hippocampus - cytology
Hippocampus - physiology
Male
Memory
Mice
Mice, Inbred C57BL
Models, Neurological
Neuroscience
Neuroscience/Animal Cognition
Neuroscience/Behavioral Neuroscience
Neuroscience/Cognitive Neuroscience
Observations
Odorants
Odors
Olfactory Pathways - physiology
Physiological aspects
Psychomotor Performance
Pyramidal Cells - cytology
Pyramidal Cells - physiology
Reaction Time - physiology
Reward
Rodents
Smell
Spatial Behavior - physiology
Spatial behavior in animals
Studies
Visual Perception - physiology
title Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-29T16%3A58%3A04IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Attention%20enhances%20the%20retrieval%20and%20stability%20of%20visuospatial%20and%20olfactory%20representations%20in%20the%20dorsal%20hippocampus&rft.jtitle=PLoS%20biology&rft.au=Muzzio,%20Isabel%20A&rft.date=2009-06-30&rft.volume=7&rft.issue=6&rft.spage=e1000140&rft.epage=e1000140&rft.pages=e1000140-e1000140&rft.issn=1545-7885&rft.eissn=1545-7885&rft_id=info:doi/10.1371/journal.pbio.1000140&rft_dat=%3Cgale_plos_%3EA638106067%3C/gale_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c665t-a197934290d44d3e5da7b5321f060af142d478162629d385769dbfd0fbe8b5563%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=67430936&rft_id=info:pmid/19564903&rft_galeid=A638106067&rfr_iscdi=true