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...
Saved in:
Published in: | PLoS biology 2009-06, Vol.7 (6), p.e1000140-e1000140 |
---|---|
Main Authors: | , , , , , , , |
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 |