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Self-Generated Movements with “Unexpected” Sensory Consequences
The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals g...
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| Published in: | Current biology 2014-09, Vol.24 (18), p.2136-2141 |
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| creator | Tiriac, Alexandre Del Rio-Bermudez, Carlos Blumberg, Mark S. |
| description | The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals generate copies, or corollary discharges, of motor commands [4, 5]. Corollary discharge facilitates the selective gating of reafferent signals arising from self-generated movements, thereby enhancing detection of novel stimuli [6–10]. However, for a developing nervous system, such sensory gating would be counterproductive if it impedes transmission of the very activity upon which activity-dependent mechanisms depend [11]. In infant rats during active (or REM) sleep—a behavioral state that predominates in early infancy [12–16]—neural circuits within the brainstem [17, 18] trigger hundreds of thousands of myoclonic twitches each day [19]. The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20–23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21–23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23]. Here, we test this hypothesis in newborn rats by manipulating the degree to which self-generated movements are expected and, therefore, their presumed recruitment of corollary discharge. We show that twitches, although self-generated, are processed as if they are unexpected.
•Reafference from REM sleep twitches, but not wake movements, triggers M1 activity•Only “unexpected” self-generated movements trigger M1 activity•Twitches are processed as if they are unexpected
It is generally assumed that all self-generated movements are accompanied by motor copies that help animals distinguish expected from unexpected sensory input. Here, in newborn rats, Tiriac et al. provide evidence for self-generated movements that are processed as if they are unexpected. Remarkably, these movements occur during REM sleep. |
| doi_str_mv | 10.1016/j.cub.2014.07.053 |
| format | article |
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•Reafference from REM sleep twitches, but not wake movements, triggers M1 activity•Only “unexpected” self-generated movements trigger M1 activity•Twitches are processed as if they are unexpected
It is generally assumed that all self-generated movements are accompanied by motor copies that help animals distinguish expected from unexpected sensory input. Here, in newborn rats, Tiriac et al. provide evidence for self-generated movements that are processed as if they are unexpected. Remarkably, these movements occur during REM sleep.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2014.07.053</identifier><identifier>PMID: 25131675</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Animals ; Female ; Male ; Motor Cortex - physiology ; Movement ; Proprioception ; Rats ; Rats, Sprague-Dawley ; Signal Transduction ; Sleep, REM</subject><ispartof>Current biology, 2014-09, Vol.24 (18), p.2136-2141</ispartof><rights>2014 Elsevier Ltd</rights><rights>Copyright © 2014 Elsevier Ltd. All rights reserved.</rights><rights>2014 Elsevier Inc. All rights reserved. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c569t-167bc50d0c77b35208ea8e043d27afc4c9fc647a0fd263a2e41b598838ec77a23</citedby><cites>FETCH-LOGICAL-c569t-167bc50d0c77b35208ea8e043d27afc4c9fc647a0fd263a2e41b598838ec77a23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25131675$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tiriac, Alexandre</creatorcontrib><creatorcontrib>Del Rio-Bermudez, Carlos</creatorcontrib><creatorcontrib>Blumberg, Mark S.</creatorcontrib><title>Self-Generated Movements with “Unexpected” Sensory Consequences</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals generate copies, or corollary discharges, of motor commands [4, 5]. Corollary discharge facilitates the selective gating of reafferent signals arising from self-generated movements, thereby enhancing detection of novel stimuli [6–10]. However, for a developing nervous system, such sensory gating would be counterproductive if it impedes transmission of the very activity upon which activity-dependent mechanisms depend [11]. In infant rats during active (or REM) sleep—a behavioral state that predominates in early infancy [12–16]—neural circuits within the brainstem [17, 18] trigger hundreds of thousands of myoclonic twitches each day [19]. The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20–23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21–23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23]. Here, we test this hypothesis in newborn rats by manipulating the degree to which self-generated movements are expected and, therefore, their presumed recruitment of corollary discharge. We show that twitches, although self-generated, are processed as if they are unexpected.
•Reafference from REM sleep twitches, but not wake movements, triggers M1 activity•Only “unexpected” self-generated movements trigger M1 activity•Twitches are processed as if they are unexpected
It is generally assumed that all self-generated movements are accompanied by motor copies that help animals distinguish expected from unexpected sensory input. Here, in newborn rats, Tiriac et al. provide evidence for self-generated movements that are processed as if they are unexpected. Remarkably, these movements occur during REM sleep.</description><subject>Animals</subject><subject>Female</subject><subject>Male</subject><subject>Motor Cortex - physiology</subject><subject>Movement</subject><subject>Proprioception</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Signal Transduction</subject><subject>Sleep, REM</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNp9kM1u1DAUhS0EaoehD9BNlSWbpNeOHduqhIRGbalUxKJ0bTnODfUoE0_tzEB3fRB4uT4JHk2pYMPqLs7PPfoIOaZQUaDN6bJym7ZiQHkFsgJRvyIzqqQugXPxmsxAN1BqxdgheZvSEoAypZsDcsgErWkjxYwsbnDoy0scMdoJu-Jz2OIKxykV3_10Vzw9_rwd8ccaXRafHn8VNzimEB-KRRgT3m9wdJjekTe9HRIePd85ub04_7r4VF5_ubxafLwunWj0VOaHrRPQgZOyrQUDhVYh8Lpj0vaOO927hksLfcea2jLktBVaqVphTlhWz8mHfe96066wc3lmtINZR7-y8cEE682_yujvzLewNZxKARnPnLx_Loghb0-TWfnkcBjsiGGTDBWN4ForWmcr3VtdDClF7F_eUDA7-GZpMnyzg29AmtyeMyd_73tJ_KGdDWd7A2ZKW4_RJOd3CDsfM2HTBf-f-t-ejZgM</recordid><startdate>20140922</startdate><enddate>20140922</enddate><creator>Tiriac, Alexandre</creator><creator>Del Rio-Bermudez, Carlos</creator><creator>Blumberg, Mark S.</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20140922</creationdate><title>Self-Generated Movements with “Unexpected” Sensory Consequences</title><author>Tiriac, Alexandre ; Del Rio-Bermudez, Carlos ; Blumberg, Mark S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c569t-167bc50d0c77b35208ea8e043d27afc4c9fc647a0fd263a2e41b598838ec77a23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Female</topic><topic>Male</topic><topic>Motor Cortex - physiology</topic><topic>Movement</topic><topic>Proprioception</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Signal Transduction</topic><topic>Sleep, REM</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tiriac, Alexandre</creatorcontrib><creatorcontrib>Del Rio-Bermudez, Carlos</creatorcontrib><creatorcontrib>Blumberg, Mark S.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tiriac, Alexandre</au><au>Del Rio-Bermudez, Carlos</au><au>Blumberg, Mark S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Self-Generated Movements with “Unexpected” Sensory Consequences</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2014-09-22</date><risdate>2014</risdate><volume>24</volume><issue>18</issue><spage>2136</spage><epage>2141</epage><pages>2136-2141</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals generate copies, or corollary discharges, of motor commands [4, 5]. Corollary discharge facilitates the selective gating of reafferent signals arising from self-generated movements, thereby enhancing detection of novel stimuli [6–10]. However, for a developing nervous system, such sensory gating would be counterproductive if it impedes transmission of the very activity upon which activity-dependent mechanisms depend [11]. In infant rats during active (or REM) sleep—a behavioral state that predominates in early infancy [12–16]—neural circuits within the brainstem [17, 18] trigger hundreds of thousands of myoclonic twitches each day [19]. The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20–23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21–23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23]. Here, we test this hypothesis in newborn rats by manipulating the degree to which self-generated movements are expected and, therefore, their presumed recruitment of corollary discharge. We show that twitches, although self-generated, are processed as if they are unexpected.
•Reafference from REM sleep twitches, but not wake movements, triggers M1 activity•Only “unexpected” self-generated movements trigger M1 activity•Twitches are processed as if they are unexpected
It is generally assumed that all self-generated movements are accompanied by motor copies that help animals distinguish expected from unexpected sensory input. Here, in newborn rats, Tiriac et al. provide evidence for self-generated movements that are processed as if they are unexpected. Remarkably, these movements occur during REM sleep.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>25131675</pmid><doi>10.1016/j.cub.2014.07.053</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Current biology, 2014-09, Vol.24 (18), p.2136-2141 |
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| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4175005 |
| source | BACON - Elsevier - GLOBAL_SCIENCEDIRECT-OPENACCESS |
| subjects | Animals Female Male Motor Cortex - physiology Movement Proprioception Rats Rats, Sprague-Dawley Signal Transduction Sleep, REM |
| title | Self-Generated Movements with “Unexpected” Sensory Consequences |
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