Multisensory coding of angular head velocity in the retrosplenial cortex
To successfully navigate the environment, animals depend on their ability to continuously track their heading direction and speed. Neurons that encode angular head velocity (AHV) are fundamental to this process, yet the contribution of various motion signals to AHV coding in the cortex remains elusi...
Gespeichert in:
Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2022-02, Vol.110 (3), p.532-543.e9 |
---|---|
Hauptverfasser: | , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 543.e9 |
---|---|
container_issue | 3 |
container_start_page | 532 |
container_title | Neuron (Cambridge, Mass.) |
container_volume | 110 |
creator | Keshavarzi, Sepiedeh Bracey, Edward F. Faville, Richard A. Campagner, Dario Tyson, Adam L. Lenzi, Stephen C. Branco, Tiago Margrie, Troy W. |
description | To successfully navigate the environment, animals depend on their ability to continuously track their heading direction and speed. Neurons that encode angular head velocity (AHV) are fundamental to this process, yet the contribution of various motion signals to AHV coding in the cortex remains elusive. By performing chronic single-unit recordings in the retrosplenial cortex (RSP) of the mouse and tracking the activity of individual AHV cells between freely moving and head-restrained conditions, we find that vestibular inputs dominate AHV signaling. Moreover, the addition of visual inputs onto these neurons increases the gain and signal-to-noise ratio of their tuning during active exploration. Psychophysical experiments and neural decoding further reveal that vestibular-visual integration increases the perceptual accuracy of angular self-motion and the fidelity of its representation by RSP ensembles. We conclude that while cortical AHV coding requires vestibular input, where possible, it also uses vision to optimize heading estimation during navigation.
•Angular head velocity (AHV) coding is widespread in the retrosplenial cortex (RSP)•AHV cells maintain their tuning during passive motion and require vestibular input•The perception of angular self-motion is improved when visual cues are present•AHV coding is similarly improved when both vestibular and visual stimuli are used
Keshavarzi et al. report that mouse retrosplenial cortical neurons can reliably track the direction and speed of head turns in complete darkness by relying on vestibular information. Addition of visual input improves perception of angular self-motion and increases the accuracy of this cortical head motion signal. |
doi_str_mv | 10.1016/j.neuron.2021.10.031 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8823706</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0896627321008461</els_id><sourcerecordid>2599070787</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3781-731d5a5e6df53734807a02fc118875f0475e093b414ee4c606b4c3d13ba09b813</originalsourceid><addsrcrecordid>eNp9UcGO0zAQtRCILQt_gFCOXFJmYie2L0hoBSzSIi5wthxn0rpy7WIn1fbvSdVlgQunkWbeezNvHmOvEdYI2L3brSPNOcV1Aw0urTVwfMJWCFrWArV-ylagdFd3jeRX7EUpOwAUrcbn7IoLqVTHmxW7_TqHyReKJeVT5dLg46ZKY2XjZg42V1uyQ3WkkJyfTpWP1bSlKtOUUzkEit6GhZQnun_Jno02FHr1UK_Zj08fv9_c1nffPn-5-XBXOy4V1pLj0NqWumFsueRCgbTQjA5RKdmOIGRLoHkvUBAJ10HXC8cH5L0F3Svk1-z9Rfcw93saHMUp22AO2e9tPplkvfl3Ev3WbNLRKNVwCd0i8PZBIKefM5XJ7H1xFIKNlOZimlZrkCCVXKDiAnWL3ZJpfFyDYM4hmJ25hGDOIZy7SwgL7c3fJz6Sfn_9jwdaHnX0lE1xnqKjwWdykxmS__-GXxrHm3U</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2599070787</pqid></control><display><type>article</type><title>Multisensory coding of angular head velocity in the retrosplenial cortex</title><source>Cell Press Free Archives</source><source>Access via ScienceDirect (Elsevier)</source><source>EZB-FREE-00999 freely available EZB journals</source><creator>Keshavarzi, Sepiedeh ; Bracey, Edward F. ; Faville, Richard A. ; Campagner, Dario ; Tyson, Adam L. ; Lenzi, Stephen C. ; Branco, Tiago ; Margrie, Troy W.</creator><creatorcontrib>Keshavarzi, Sepiedeh ; Bracey, Edward F. ; Faville, Richard A. ; Campagner, Dario ; Tyson, Adam L. ; Lenzi, Stephen C. ; Branco, Tiago ; Margrie, Troy W.</creatorcontrib><description>To successfully navigate the environment, animals depend on their ability to continuously track their heading direction and speed. Neurons that encode angular head velocity (AHV) are fundamental to this process, yet the contribution of various motion signals to AHV coding in the cortex remains elusive. By performing chronic single-unit recordings in the retrosplenial cortex (RSP) of the mouse and tracking the activity of individual AHV cells between freely moving and head-restrained conditions, we find that vestibular inputs dominate AHV signaling. Moreover, the addition of visual inputs onto these neurons increases the gain and signal-to-noise ratio of their tuning during active exploration. Psychophysical experiments and neural decoding further reveal that vestibular-visual integration increases the perceptual accuracy of angular self-motion and the fidelity of its representation by RSP ensembles. We conclude that while cortical AHV coding requires vestibular input, where possible, it also uses vision to optimize heading estimation during navigation.
•Angular head velocity (AHV) coding is widespread in the retrosplenial cortex (RSP)•AHV cells maintain their tuning during passive motion and require vestibular input•The perception of angular self-motion is improved when visual cues are present•AHV coding is similarly improved when both vestibular and visual stimuli are used
Keshavarzi et al. report that mouse retrosplenial cortical neurons can reliably track the direction and speed of head turns in complete darkness by relying on vestibular information. Addition of visual input improves perception of angular self-motion and increases the accuracy of this cortical head motion signal.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2021.10.031</identifier><identifier>PMID: 34788632</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Angular head velocity ; Head direction ; Multisensory integration ; Navigation ; Optic flow ; Retrosplenial cortex ; Self-motion ; Spatial orientation ; Vestibular sense</subject><ispartof>Neuron (Cambridge, Mass.), 2022-02, Vol.110 (3), p.532-543.e9</ispartof><rights>2021 The Authors</rights><rights>Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.</rights><rights>2021 The Authors 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3781-731d5a5e6df53734807a02fc118875f0475e093b414ee4c606b4c3d13ba09b813</citedby><cites>FETCH-LOGICAL-c3781-731d5a5e6df53734807a02fc118875f0475e093b414ee4c606b4c3d13ba09b813</cites><orcidid>0000-0002-7310-8034</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuron.2021.10.031$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34788632$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Keshavarzi, Sepiedeh</creatorcontrib><creatorcontrib>Bracey, Edward F.</creatorcontrib><creatorcontrib>Faville, Richard A.</creatorcontrib><creatorcontrib>Campagner, Dario</creatorcontrib><creatorcontrib>Tyson, Adam L.</creatorcontrib><creatorcontrib>Lenzi, Stephen C.</creatorcontrib><creatorcontrib>Branco, Tiago</creatorcontrib><creatorcontrib>Margrie, Troy W.</creatorcontrib><title>Multisensory coding of angular head velocity in the retrosplenial cortex</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>To successfully navigate the environment, animals depend on their ability to continuously track their heading direction and speed. Neurons that encode angular head velocity (AHV) are fundamental to this process, yet the contribution of various motion signals to AHV coding in the cortex remains elusive. By performing chronic single-unit recordings in the retrosplenial cortex (RSP) of the mouse and tracking the activity of individual AHV cells between freely moving and head-restrained conditions, we find that vestibular inputs dominate AHV signaling. Moreover, the addition of visual inputs onto these neurons increases the gain and signal-to-noise ratio of their tuning during active exploration. Psychophysical experiments and neural decoding further reveal that vestibular-visual integration increases the perceptual accuracy of angular self-motion and the fidelity of its representation by RSP ensembles. We conclude that while cortical AHV coding requires vestibular input, where possible, it also uses vision to optimize heading estimation during navigation.
•Angular head velocity (AHV) coding is widespread in the retrosplenial cortex (RSP)•AHV cells maintain their tuning during passive motion and require vestibular input•The perception of angular self-motion is improved when visual cues are present•AHV coding is similarly improved when both vestibular and visual stimuli are used
Keshavarzi et al. report that mouse retrosplenial cortical neurons can reliably track the direction and speed of head turns in complete darkness by relying on vestibular information. Addition of visual input improves perception of angular self-motion and increases the accuracy of this cortical head motion signal.</description><subject>Angular head velocity</subject><subject>Head direction</subject><subject>Multisensory integration</subject><subject>Navigation</subject><subject>Optic flow</subject><subject>Retrosplenial cortex</subject><subject>Self-motion</subject><subject>Spatial orientation</subject><subject>Vestibular sense</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9UcGO0zAQtRCILQt_gFCOXFJmYie2L0hoBSzSIi5wthxn0rpy7WIn1fbvSdVlgQunkWbeezNvHmOvEdYI2L3brSPNOcV1Aw0urTVwfMJWCFrWArV-ylagdFd3jeRX7EUpOwAUrcbn7IoLqVTHmxW7_TqHyReKJeVT5dLg46ZKY2XjZg42V1uyQ3WkkJyfTpWP1bSlKtOUUzkEit6GhZQnun_Jno02FHr1UK_Zj08fv9_c1nffPn-5-XBXOy4V1pLj0NqWumFsueRCgbTQjA5RKdmOIGRLoHkvUBAJ10HXC8cH5L0F3Svk1-z9Rfcw93saHMUp22AO2e9tPplkvfl3Ev3WbNLRKNVwCd0i8PZBIKefM5XJ7H1xFIKNlOZimlZrkCCVXKDiAnWL3ZJpfFyDYM4hmJ25hGDOIZy7SwgL7c3fJz6Sfn_9jwdaHnX0lE1xnqKjwWdykxmS__-GXxrHm3U</recordid><startdate>20220202</startdate><enddate>20220202</enddate><creator>Keshavarzi, Sepiedeh</creator><creator>Bracey, Edward F.</creator><creator>Faville, Richard A.</creator><creator>Campagner, Dario</creator><creator>Tyson, Adam L.</creator><creator>Lenzi, Stephen C.</creator><creator>Branco, Tiago</creator><creator>Margrie, Troy W.</creator><general>Elsevier Inc</general><general>Cell Press</general><scope>6I.</scope><scope>AAFTH</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7310-8034</orcidid></search><sort><creationdate>20220202</creationdate><title>Multisensory coding of angular head velocity in the retrosplenial cortex</title><author>Keshavarzi, Sepiedeh ; Bracey, Edward F. ; Faville, Richard A. ; Campagner, Dario ; Tyson, Adam L. ; Lenzi, Stephen C. ; Branco, Tiago ; Margrie, Troy W.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3781-731d5a5e6df53734807a02fc118875f0475e093b414ee4c606b4c3d13ba09b813</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Angular head velocity</topic><topic>Head direction</topic><topic>Multisensory integration</topic><topic>Navigation</topic><topic>Optic flow</topic><topic>Retrosplenial cortex</topic><topic>Self-motion</topic><topic>Spatial orientation</topic><topic>Vestibular sense</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Keshavarzi, Sepiedeh</creatorcontrib><creatorcontrib>Bracey, Edward F.</creatorcontrib><creatorcontrib>Faville, Richard A.</creatorcontrib><creatorcontrib>Campagner, Dario</creatorcontrib><creatorcontrib>Tyson, Adam L.</creatorcontrib><creatorcontrib>Lenzi, Stephen C.</creatorcontrib><creatorcontrib>Branco, Tiago</creatorcontrib><creatorcontrib>Margrie, Troy W.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Keshavarzi, Sepiedeh</au><au>Bracey, Edward F.</au><au>Faville, Richard A.</au><au>Campagner, Dario</au><au>Tyson, Adam L.</au><au>Lenzi, Stephen C.</au><au>Branco, Tiago</au><au>Margrie, Troy W.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Multisensory coding of angular head velocity in the retrosplenial cortex</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2022-02-02</date><risdate>2022</risdate><volume>110</volume><issue>3</issue><spage>532</spage><epage>543.e9</epage><pages>532-543.e9</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>To successfully navigate the environment, animals depend on their ability to continuously track their heading direction and speed. Neurons that encode angular head velocity (AHV) are fundamental to this process, yet the contribution of various motion signals to AHV coding in the cortex remains elusive. By performing chronic single-unit recordings in the retrosplenial cortex (RSP) of the mouse and tracking the activity of individual AHV cells between freely moving and head-restrained conditions, we find that vestibular inputs dominate AHV signaling. Moreover, the addition of visual inputs onto these neurons increases the gain and signal-to-noise ratio of their tuning during active exploration. Psychophysical experiments and neural decoding further reveal that vestibular-visual integration increases the perceptual accuracy of angular self-motion and the fidelity of its representation by RSP ensembles. We conclude that while cortical AHV coding requires vestibular input, where possible, it also uses vision to optimize heading estimation during navigation.
•Angular head velocity (AHV) coding is widespread in the retrosplenial cortex (RSP)•AHV cells maintain their tuning during passive motion and require vestibular input•The perception of angular self-motion is improved when visual cues are present•AHV coding is similarly improved when both vestibular and visual stimuli are used
Keshavarzi et al. report that mouse retrosplenial cortical neurons can reliably track the direction and speed of head turns in complete darkness by relying on vestibular information. Addition of visual input improves perception of angular self-motion and increases the accuracy of this cortical head motion signal.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34788632</pmid><doi>10.1016/j.neuron.2021.10.031</doi><orcidid>https://orcid.org/0000-0002-7310-8034</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0896-6273 |
ispartof | Neuron (Cambridge, Mass.), 2022-02, Vol.110 (3), p.532-543.e9 |
issn | 0896-6273 1097-4199 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8823706 |
source | Cell Press Free Archives; Access via ScienceDirect (Elsevier); EZB-FREE-00999 freely available EZB journals |
subjects | Angular head velocity Head direction Multisensory integration Navigation Optic flow Retrosplenial cortex Self-motion Spatial orientation Vestibular sense |
title | Multisensory coding of angular head velocity in the retrosplenial cortex |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-25T13%3A00%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Multisensory%20coding%20of%20angular%20head%20velocity%20in%20the%20retrosplenial%20cortex&rft.jtitle=Neuron%20(Cambridge,%20Mass.)&rft.au=Keshavarzi,%20Sepiedeh&rft.date=2022-02-02&rft.volume=110&rft.issue=3&rft.spage=532&rft.epage=543.e9&rft.pages=532-543.e9&rft.issn=0896-6273&rft.eissn=1097-4199&rft_id=info:doi/10.1016/j.neuron.2021.10.031&rft_dat=%3Cproquest_pubme%3E2599070787%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2599070787&rft_id=info:pmid/34788632&rft_els_id=S0896627321008461&rfr_iscdi=true |