Inhibitory interneurons in a brainstem circuit adjust their inhibitory motifs to process multimodal input
Key points Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information. T...
Gespeichert in:
Veröffentlicht in: | The Journal of physiology 2021-01, Vol.599 (2), p.631-645 |
---|---|
Hauptverfasser: | , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 645 |
---|---|
container_issue | 2 |
container_start_page | 631 |
container_title | The Journal of physiology |
container_volume | 599 |
creator | Wu, Calvin Shore, Susan E. |
description | Key points
Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information.
The present study applies a statistical method to in vivo multichannel spike trains of dorsal cochlear nucleus neurons to disentangle reciprocal and feedforward‐inhibitory motifs.
After inducing input‐specific plasticity, reciprocal and feedforward inhibition are found to be differentially regulated, and the combined effect synergistically modulates circuit output.
The findings highlight the interplay among different circuit motifs as a key element in neural computation.
Inhibitory interneurons play an essential role in neural computations by utilizing a combination of reciprocal (interneurons inhibiting each other) and feedforward (interneuron inhibiting the principal neuron) inhibition to process information. To disentangle the interplay between the two inhibitory‐circuit motifs and understand their effects on the circuit output, in vivo recordings were made from the guinea pig dorsal cochlear nucleus, a cerebellar‐like brainstem circuit. Spikes from inhibitory interneurons (cartwheel cell) and principal output neurons (fusiform cell) were compared before and after manipulating their common multimodal input. Using a statistical model based on the Cox method of modulated renewal process of spike train influence, reciprocal‐ and feedforward‐inhibition motifs were quantified. In response to altered multimodal input, reciprocal inhibition was strengthened while feedforward inhibition was weakened, and the two motifs combined to modulate fusiform cell output and acoustic‐driven responses. These findings reveal the cartwheel cell's role in auditory and multimodal processing, as well as illustrated the balance between different inhibitory‐circuit motifs as a key element in neural computation.
Key points
Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information.
The present study applies a statistical method to in vivo multichannel spike trains of dorsal cochlear nucleus neurons to disentangle reciprocal and feedforward‐inhibitory motifs.
After |
doi_str_mv | 10.1113/JP280741 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7855092</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2454407949</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4398-8edf700275baba5ebbbddfd4d6cc8a5599371494f5bef97dca65086069bb30643</originalsourceid><addsrcrecordid>eNp1kV1rFDEUhoModq1Cf4EEvPFmajJJJpObQlmqthTsRb0O-Ro3y0yy5qNl_72RtmsVvAqHPOfhTV4ATjA6xRiTT1c3_Yg4xS_ACtNBdJwL8hKsEOr7jnCGj8CbnLcIYYKEeA2OCMGI9JStgL8MG699iWkPfSguBVdTDLkNUEGdlA-5uAUan0z1BSq7rbnAsnE-Neawu8TipwxLhLsUjcsZLnUufolWzY3b1fIWvJrUnN27x_MYfP98cbv-2l1_-3K5Pr_uDCVi7EZnJ96Cc6aVVsxpra2dLLWDMaNiTAjCMRV0YtpNglujBobGAQ1Ca4IGSo7B2YN3V_XirHGhJDXLXfKLSnsZlZd_3wS_kT_ineQjY0j0TfDxUZDiz-pykYvPxs2zCi7WLNu_UYq4oKKhH_5Bt7Gm0J7XKM7HVgYTf4QmxZyTmw5hMJK_-5NP_TX0_fPwB_CpsAacPgD3fnb7_4rk7dUNppSO5BcukqZI</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2477814659</pqid></control><display><type>article</type><title>Inhibitory interneurons in a brainstem circuit adjust their inhibitory motifs to process multimodal input</title><source>MEDLINE</source><source>Wiley Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Wiley Free Content</source><source>PubMed Central</source><creator>Wu, Calvin ; Shore, Susan E.</creator><creatorcontrib>Wu, Calvin ; Shore, Susan E.</creatorcontrib><description>Key points
Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information.
The present study applies a statistical method to in vivo multichannel spike trains of dorsal cochlear nucleus neurons to disentangle reciprocal and feedforward‐inhibitory motifs.
After inducing input‐specific plasticity, reciprocal and feedforward inhibition are found to be differentially regulated, and the combined effect synergistically modulates circuit output.
The findings highlight the interplay among different circuit motifs as a key element in neural computation.
Inhibitory interneurons play an essential role in neural computations by utilizing a combination of reciprocal (interneurons inhibiting each other) and feedforward (interneuron inhibiting the principal neuron) inhibition to process information. To disentangle the interplay between the two inhibitory‐circuit motifs and understand their effects on the circuit output, in vivo recordings were made from the guinea pig dorsal cochlear nucleus, a cerebellar‐like brainstem circuit. Spikes from inhibitory interneurons (cartwheel cell) and principal output neurons (fusiform cell) were compared before and after manipulating their common multimodal input. Using a statistical model based on the Cox method of modulated renewal process of spike train influence, reciprocal‐ and feedforward‐inhibition motifs were quantified. In response to altered multimodal input, reciprocal inhibition was strengthened while feedforward inhibition was weakened, and the two motifs combined to modulate fusiform cell output and acoustic‐driven responses. These findings reveal the cartwheel cell's role in auditory and multimodal processing, as well as illustrated the balance between different inhibitory‐circuit motifs as a key element in neural computation.
Key points
Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information.
The present study applies a statistical method to in vivo multichannel spike trains of dorsal cochlear nucleus neurons to disentangle reciprocal and feedforward‐inhibitory motifs.
After inducing input‐specific plasticity, reciprocal and feedforward inhibition are found to be differentially regulated, and the combined effect synergistically modulates circuit output.
The findings highlight the interplay among different circuit motifs as a key element in neural computation.</description><identifier>ISSN: 0022-3751</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/JP280741</identifier><identifier>PMID: 33103245</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Animals ; Brain stem ; Cerebellum ; Cochlea ; Cochlear nuclei ; Cochlear Nucleus ; dorsal cochlear nucleus ; functional connectivity ; Guinea Pigs ; Information processing ; Interneurons ; Mathematical models ; multichannel spike train ; Neural Inhibition ; Neurons</subject><ispartof>The Journal of physiology, 2021-01, Vol.599 (2), p.631-645</ispartof><rights>2020 The Authors. The Journal of Physiology © 2020 The Physiological Society</rights><rights>2020 The Authors. The Journal of Physiology © 2020 The Physiological Society.</rights><rights>Journal compilation © 2021 The Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4398-8edf700275baba5ebbbddfd4d6cc8a5599371494f5bef97dca65086069bb30643</citedby><cites>FETCH-LOGICAL-c4398-8edf700275baba5ebbbddfd4d6cc8a5599371494f5bef97dca65086069bb30643</cites><orcidid>0000-0002-5300-5492 ; 0000-0002-2622-0576</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7855092/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7855092/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33103245$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Calvin</creatorcontrib><creatorcontrib>Shore, Susan E.</creatorcontrib><title>Inhibitory interneurons in a brainstem circuit adjust their inhibitory motifs to process multimodal input</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>Key points
Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information.
The present study applies a statistical method to in vivo multichannel spike trains of dorsal cochlear nucleus neurons to disentangle reciprocal and feedforward‐inhibitory motifs.
After inducing input‐specific plasticity, reciprocal and feedforward inhibition are found to be differentially regulated, and the combined effect synergistically modulates circuit output.
The findings highlight the interplay among different circuit motifs as a key element in neural computation.
Inhibitory interneurons play an essential role in neural computations by utilizing a combination of reciprocal (interneurons inhibiting each other) and feedforward (interneuron inhibiting the principal neuron) inhibition to process information. To disentangle the interplay between the two inhibitory‐circuit motifs and understand their effects on the circuit output, in vivo recordings were made from the guinea pig dorsal cochlear nucleus, a cerebellar‐like brainstem circuit. Spikes from inhibitory interneurons (cartwheel cell) and principal output neurons (fusiform cell) were compared before and after manipulating their common multimodal input. Using a statistical model based on the Cox method of modulated renewal process of spike train influence, reciprocal‐ and feedforward‐inhibition motifs were quantified. In response to altered multimodal input, reciprocal inhibition was strengthened while feedforward inhibition was weakened, and the two motifs combined to modulate fusiform cell output and acoustic‐driven responses. These findings reveal the cartwheel cell's role in auditory and multimodal processing, as well as illustrated the balance between different inhibitory‐circuit motifs as a key element in neural computation.
Key points
Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information.
The present study applies a statistical method to in vivo multichannel spike trains of dorsal cochlear nucleus neurons to disentangle reciprocal and feedforward‐inhibitory motifs.
After inducing input‐specific plasticity, reciprocal and feedforward inhibition are found to be differentially regulated, and the combined effect synergistically modulates circuit output.
The findings highlight the interplay among different circuit motifs as a key element in neural computation.</description><subject>Animals</subject><subject>Brain stem</subject><subject>Cerebellum</subject><subject>Cochlea</subject><subject>Cochlear nuclei</subject><subject>Cochlear Nucleus</subject><subject>dorsal cochlear nucleus</subject><subject>functional connectivity</subject><subject>Guinea Pigs</subject><subject>Information processing</subject><subject>Interneurons</subject><subject>Mathematical models</subject><subject>multichannel spike train</subject><subject>Neural Inhibition</subject><subject>Neurons</subject><issn>0022-3751</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kV1rFDEUhoModq1Cf4EEvPFmajJJJpObQlmqthTsRb0O-Ro3y0yy5qNl_72RtmsVvAqHPOfhTV4ATjA6xRiTT1c3_Yg4xS_ACtNBdJwL8hKsEOr7jnCGj8CbnLcIYYKEeA2OCMGI9JStgL8MG699iWkPfSguBVdTDLkNUEGdlA-5uAUan0z1BSq7rbnAsnE-Neawu8TipwxLhLsUjcsZLnUufolWzY3b1fIWvJrUnN27x_MYfP98cbv-2l1_-3K5Pr_uDCVi7EZnJ96Cc6aVVsxpra2dLLWDMaNiTAjCMRV0YtpNglujBobGAQ1Ca4IGSo7B2YN3V_XirHGhJDXLXfKLSnsZlZd_3wS_kT_ineQjY0j0TfDxUZDiz-pykYvPxs2zCi7WLNu_UYq4oKKhH_5Bt7Gm0J7XKM7HVgYTf4QmxZyTmw5hMJK_-5NP_TX0_fPwB_CpsAacPgD3fnb7_4rk7dUNppSO5BcukqZI</recordid><startdate>20210101</startdate><enddate>20210101</enddate><creator>Wu, Calvin</creator><creator>Shore, Susan E.</creator><general>Wiley Subscription Services, Inc</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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5300-5492</orcidid><orcidid>https://orcid.org/0000-0002-2622-0576</orcidid></search><sort><creationdate>20210101</creationdate><title>Inhibitory interneurons in a brainstem circuit adjust their inhibitory motifs to process multimodal input</title><author>Wu, Calvin ; Shore, Susan E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4398-8edf700275baba5ebbbddfd4d6cc8a5599371494f5bef97dca65086069bb30643</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Brain stem</topic><topic>Cerebellum</topic><topic>Cochlea</topic><topic>Cochlear nuclei</topic><topic>Cochlear Nucleus</topic><topic>dorsal cochlear nucleus</topic><topic>functional connectivity</topic><topic>Guinea Pigs</topic><topic>Information processing</topic><topic>Interneurons</topic><topic>Mathematical models</topic><topic>multichannel spike train</topic><topic>Neural Inhibition</topic><topic>Neurons</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Calvin</creatorcontrib><creatorcontrib>Shore, Susan E.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Calvin</au><au>Shore, Susan E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inhibitory interneurons in a brainstem circuit adjust their inhibitory motifs to process multimodal input</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2021-01-01</date><risdate>2021</risdate><volume>599</volume><issue>2</issue><spage>631</spage><epage>645</epage><pages>631-645</pages><issn>0022-3751</issn><eissn>1469-7793</eissn><abstract>Key points
Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information.
The present study applies a statistical method to in vivo multichannel spike trains of dorsal cochlear nucleus neurons to disentangle reciprocal and feedforward‐inhibitory motifs.
After inducing input‐specific plasticity, reciprocal and feedforward inhibition are found to be differentially regulated, and the combined effect synergistically modulates circuit output.
The findings highlight the interplay among different circuit motifs as a key element in neural computation.
Inhibitory interneurons play an essential role in neural computations by utilizing a combination of reciprocal (interneurons inhibiting each other) and feedforward (interneuron inhibiting the principal neuron) inhibition to process information. To disentangle the interplay between the two inhibitory‐circuit motifs and understand their effects on the circuit output, in vivo recordings were made from the guinea pig dorsal cochlear nucleus, a cerebellar‐like brainstem circuit. Spikes from inhibitory interneurons (cartwheel cell) and principal output neurons (fusiform cell) were compared before and after manipulating their common multimodal input. Using a statistical model based on the Cox method of modulated renewal process of spike train influence, reciprocal‐ and feedforward‐inhibition motifs were quantified. In response to altered multimodal input, reciprocal inhibition was strengthened while feedforward inhibition was weakened, and the two motifs combined to modulate fusiform cell output and acoustic‐driven responses. These findings reveal the cartwheel cell's role in auditory and multimodal processing, as well as illustrated the balance between different inhibitory‐circuit motifs as a key element in neural computation.
Key points
Inhibitory‐interneuron networks, consisting of multiple forms of circuit motifs including reciprocal (inhibitory interneurons inhibiting other interneurons) and feedforward (inhibitory interneurons inhibiting principal neurons) connections, are crucial in processing sensory information.
The present study applies a statistical method to in vivo multichannel spike trains of dorsal cochlear nucleus neurons to disentangle reciprocal and feedforward‐inhibitory motifs.
After inducing input‐specific plasticity, reciprocal and feedforward inhibition are found to be differentially regulated, and the combined effect synergistically modulates circuit output.
The findings highlight the interplay among different circuit motifs as a key element in neural computation.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>33103245</pmid><doi>10.1113/JP280741</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-5300-5492</orcidid><orcidid>https://orcid.org/0000-0002-2622-0576</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0022-3751 |
ispartof | The Journal of physiology, 2021-01, Vol.599 (2), p.631-645 |
issn | 0022-3751 1469-7793 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7855092 |
source | MEDLINE; Wiley Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Free Content; PubMed Central |
subjects | Animals Brain stem Cerebellum Cochlea Cochlear nuclei Cochlear Nucleus dorsal cochlear nucleus functional connectivity Guinea Pigs Information processing Interneurons Mathematical models multichannel spike train Neural Inhibition Neurons |
title | Inhibitory interneurons in a brainstem circuit adjust their inhibitory motifs to process multimodal input |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-05T01%3A55%3A18IST&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=Inhibitory%20interneurons%20in%20a%20brainstem%20circuit%20adjust%20their%20inhibitory%20motifs%20to%20process%20multimodal%20input&rft.jtitle=The%20Journal%20of%20physiology&rft.au=Wu,%20Calvin&rft.date=2021-01-01&rft.volume=599&rft.issue=2&rft.spage=631&rft.epage=645&rft.pages=631-645&rft.issn=0022-3751&rft.eissn=1469-7793&rft_id=info:doi/10.1113/JP280741&rft_dat=%3Cproquest_pubme%3E2454407949%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=2477814659&rft_id=info:pmid/33103245&rfr_iscdi=true |