No Evidence for Entrainment: Endogenous Gamma Oscillations and Rhythmic Flicker Responses Coexist in Visual Cortex
Over the past decades, numerous studies have linked cortical gamma oscillations (∼30-100 Hz) to neurocomputational mechanisms. Their functional relevance, however, is still passionately debated. Here, we asked whether endogenous gamma oscillations in the human brain can be entrained by a rhythmic ph...
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description | Over the past decades, numerous studies have linked cortical gamma oscillations (∼30-100 Hz) to neurocomputational mechanisms. Their functional relevance, however, is still passionately debated. Here, we asked whether endogenous gamma oscillations in the human brain can be entrained by a rhythmic photic drive >50 Hz. Such a noninvasive modulation of endogenous brain rhythms would allow conclusions about their causal involvement in neurocognition. To this end, we systematically investigated oscillatory responses to a rapid sinusoidal flicker in the absence and presence of endogenous gamma oscillations using magnetoencephalography (MEG) in combination with a high-frequency projector. The photic drive produced a robust response over visual cortex to stimulation frequencies of up to 80 Hz. Strong, endogenous gamma oscillations were induced using moving grating stimuli as repeatedly done in previous research. When superimposing the flicker and the gratings, there was no evidence for phase or frequency entrainment of the endogenous gamma oscillations by the photic drive. Unexpectedly, we did not observe an amplification of the flicker response around participants' individual gamma frequencies (IGFs); rather, the magnitude of the response decreased monotonically with increasing frequency. Source reconstruction suggests that the flicker response and the gamma oscillations were produced by separate, coexistent generators in visual cortex. The presented findings challenge the notion that cortical gamma oscillations can be entrained by rhythmic visual stimulation. Instead, the mechanism generating endogenous gamma oscillations seems to be resilient to external perturbation.
We aimed to investigate to what extent ongoing, high-frequency oscillations in the gamma-band (30-100 Hz) in the human brain can be entrained by a visual flicker. Gamma oscillations have long been suggested to coordinate neuronal firing and enable interregional communication. Our results demonstrate that rhythmic visual stimulation cannot hijack the dynamics of ongoing gamma oscillations; rather, the flicker response and the endogenous gamma oscillations coexist in different visual areas. Therefore, while a visual flicker evokes a strong neuronal response even at high frequencies in the gamma-band, it does not entrain endogenous gamma oscillations in visual cortex. This has important implications for interpreting studies investigating the causal and neuroprotective effects of rhythmic sensory stim |
doi_str_mv | 10.1523/JNEUROSCI.3134-20.2021 |
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We aimed to investigate to what extent ongoing, high-frequency oscillations in the gamma-band (30-100 Hz) in the human brain can be entrained by a visual flicker. Gamma oscillations have long been suggested to coordinate neuronal firing and enable interregional communication. Our results demonstrate that rhythmic visual stimulation cannot hijack the dynamics of ongoing gamma oscillations; rather, the flicker response and the endogenous gamma oscillations coexist in different visual areas. Therefore, while a visual flicker evokes a strong neuronal response even at high frequencies in the gamma-band, it does not entrain endogenous gamma oscillations in visual cortex. This has important implications for interpreting studies investigating the causal and neuroprotective effects of rhythmic sensory stimulation in the gamma-band.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.3134-20.2021</identifier><identifier>PMID: 34230106</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Adult ; Biological Clocks - physiology ; Brain ; Brain Mapping - methods ; Cognitive science ; Entrainment ; Female ; Flicker ; Gamma Rhythm - physiology ; Humans ; Magnetoencephalography ; Magnetoencephalography - methods ; Male ; Oscillations ; Perturbation ; Photic Stimulation ; Rhythms ; Stimulation ; Visual cortex ; Visual Cortex - physiology ; Visual Perception - physiology ; Visual stimuli</subject><ispartof>The Journal of neuroscience, 2021-08, Vol.41 (31), p.6684-6698</ispartof><rights>Copyright © 2021 Duecker et al.</rights><rights>Copyright Society for Neuroscience Aug 4, 2021</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2021 Duecker et al. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c476t-3fca6d579ff59f4acdb91251970ce6c6b1f4857a09caa6f651bc7c3b1d3cf273</citedby><orcidid>0000-0001-7887-3395 ; 0000-0003-0323-2272 ; 0000-0001-8193-8348 ; 0000-0002-0934-418X</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/PMC8336697/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8336697/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34230106$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04914795$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Duecker, Katharina</creatorcontrib><creatorcontrib>Gutteling, Tjerk P</creatorcontrib><creatorcontrib>Herrmann, Christoph S</creatorcontrib><creatorcontrib>Jensen, Ole</creatorcontrib><title>No Evidence for Entrainment: Endogenous Gamma Oscillations and Rhythmic Flicker Responses Coexist in Visual Cortex</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Over the past decades, numerous studies have linked cortical gamma oscillations (∼30-100 Hz) to neurocomputational mechanisms. Their functional relevance, however, is still passionately debated. Here, we asked whether endogenous gamma oscillations in the human brain can be entrained by a rhythmic photic drive >50 Hz. Such a noninvasive modulation of endogenous brain rhythms would allow conclusions about their causal involvement in neurocognition. To this end, we systematically investigated oscillatory responses to a rapid sinusoidal flicker in the absence and presence of endogenous gamma oscillations using magnetoencephalography (MEG) in combination with a high-frequency projector. The photic drive produced a robust response over visual cortex to stimulation frequencies of up to 80 Hz. Strong, endogenous gamma oscillations were induced using moving grating stimuli as repeatedly done in previous research. When superimposing the flicker and the gratings, there was no evidence for phase or frequency entrainment of the endogenous gamma oscillations by the photic drive. Unexpectedly, we did not observe an amplification of the flicker response around participants' individual gamma frequencies (IGFs); rather, the magnitude of the response decreased monotonically with increasing frequency. Source reconstruction suggests that the flicker response and the gamma oscillations were produced by separate, coexistent generators in visual cortex. The presented findings challenge the notion that cortical gamma oscillations can be entrained by rhythmic visual stimulation. Instead, the mechanism generating endogenous gamma oscillations seems to be resilient to external perturbation.
We aimed to investigate to what extent ongoing, high-frequency oscillations in the gamma-band (30-100 Hz) in the human brain can be entrained by a visual flicker. Gamma oscillations have long been suggested to coordinate neuronal firing and enable interregional communication. Our results demonstrate that rhythmic visual stimulation cannot hijack the dynamics of ongoing gamma oscillations; rather, the flicker response and the endogenous gamma oscillations coexist in different visual areas. Therefore, while a visual flicker evokes a strong neuronal response even at high frequencies in the gamma-band, it does not entrain endogenous gamma oscillations in visual cortex. This has important implications for interpreting studies investigating the causal and neuroprotective effects of rhythmic sensory stimulation in the gamma-band.</description><subject>Adult</subject><subject>Biological Clocks - physiology</subject><subject>Brain</subject><subject>Brain Mapping - methods</subject><subject>Cognitive science</subject><subject>Entrainment</subject><subject>Female</subject><subject>Flicker</subject><subject>Gamma Rhythm - physiology</subject><subject>Humans</subject><subject>Magnetoencephalography</subject><subject>Magnetoencephalography - methods</subject><subject>Male</subject><subject>Oscillations</subject><subject>Perturbation</subject><subject>Photic Stimulation</subject><subject>Rhythms</subject><subject>Stimulation</subject><subject>Visual cortex</subject><subject>Visual Cortex - physiology</subject><subject>Visual Perception - physiology</subject><subject>Visual stimuli</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkk1vGyEQhlHVqnHT_oUIqZf2sA5fC6GHSpHlfMmKJTftFbEsxKS74MDaSv59WTm12pwQ8z4zwwwvACcYTXFN6OnN7fznavljdj2lmLKKoClBBL8Bk6LKijCE34IJIgJVnAl2BD7k_IAQEgiL9-CIMkIRRnwC0m2E851vbTAWupjgPAxJ-9DbMHwrlzbe2xC3GV7qvtdwmY3vOj34GDLUoYWr9fOw7r2BF503v22CK5s3RbQZzqJ98nmAPsBfPm91VyJpsE8fwTunu2w_vZzH4O5ifje7qhbLy-vZ-aIyTPChos5o3tZCOldLx7RpG4lJjaVAxnLDG-zYWS00kkZr7niNGyMMbXBLjSOCHoPv-7KbbdPb1thxsE5tku91elZRe_W_Evxa3cedOqOUczkW-LovsH6VdnW-UGMMMYmZkPUOF_bLS7MUH7c2D6r32diyqmDL9hSpmSSIc8QK-vkV-hC3KZRNFKoAGEtJC8X3lEkx52Td4QUYqdEB6uAANTpAEaRGB5TEk3_HPqT9_XL6B0yOrtw</recordid><startdate>20210804</startdate><enddate>20210804</enddate><creator>Duecker, Katharina</creator><creator>Gutteling, Tjerk P</creator><creator>Herrmann, Christoph S</creator><creator>Jensen, Ole</creator><general>Society for Neuroscience</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>7QG</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7887-3395</orcidid><orcidid>https://orcid.org/0000-0003-0323-2272</orcidid><orcidid>https://orcid.org/0000-0001-8193-8348</orcidid><orcidid>https://orcid.org/0000-0002-0934-418X</orcidid></search><sort><creationdate>20210804</creationdate><title>No Evidence for Entrainment: Endogenous Gamma Oscillations and Rhythmic Flicker Responses Coexist in Visual Cortex</title><author>Duecker, Katharina ; Gutteling, Tjerk P ; Herrmann, Christoph S ; Jensen, Ole</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c476t-3fca6d579ff59f4acdb91251970ce6c6b1f4857a09caa6f651bc7c3b1d3cf273</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adult</topic><topic>Biological Clocks - physiology</topic><topic>Brain</topic><topic>Brain Mapping - methods</topic><topic>Cognitive science</topic><topic>Entrainment</topic><topic>Female</topic><topic>Flicker</topic><topic>Gamma Rhythm - physiology</topic><topic>Humans</topic><topic>Magnetoencephalography</topic><topic>Magnetoencephalography - methods</topic><topic>Male</topic><topic>Oscillations</topic><topic>Perturbation</topic><topic>Photic Stimulation</topic><topic>Rhythms</topic><topic>Stimulation</topic><topic>Visual cortex</topic><topic>Visual Cortex - physiology</topic><topic>Visual Perception - physiology</topic><topic>Visual stimuli</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Duecker, Katharina</creatorcontrib><creatorcontrib>Gutteling, Tjerk P</creatorcontrib><creatorcontrib>Herrmann, Christoph S</creatorcontrib><creatorcontrib>Jensen, Ole</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Duecker, Katharina</au><au>Gutteling, Tjerk P</au><au>Herrmann, Christoph S</au><au>Jensen, Ole</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>No Evidence for Entrainment: Endogenous Gamma Oscillations and Rhythmic Flicker Responses Coexist in Visual Cortex</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2021-08-04</date><risdate>2021</risdate><volume>41</volume><issue>31</issue><spage>6684</spage><epage>6698</epage><pages>6684-6698</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Over the past decades, numerous studies have linked cortical gamma oscillations (∼30-100 Hz) to neurocomputational mechanisms. Their functional relevance, however, is still passionately debated. Here, we asked whether endogenous gamma oscillations in the human brain can be entrained by a rhythmic photic drive >50 Hz. Such a noninvasive modulation of endogenous brain rhythms would allow conclusions about their causal involvement in neurocognition. To this end, we systematically investigated oscillatory responses to a rapid sinusoidal flicker in the absence and presence of endogenous gamma oscillations using magnetoencephalography (MEG) in combination with a high-frequency projector. The photic drive produced a robust response over visual cortex to stimulation frequencies of up to 80 Hz. Strong, endogenous gamma oscillations were induced using moving grating stimuli as repeatedly done in previous research. When superimposing the flicker and the gratings, there was no evidence for phase or frequency entrainment of the endogenous gamma oscillations by the photic drive. Unexpectedly, we did not observe an amplification of the flicker response around participants' individual gamma frequencies (IGFs); rather, the magnitude of the response decreased monotonically with increasing frequency. Source reconstruction suggests that the flicker response and the gamma oscillations were produced by separate, coexistent generators in visual cortex. The presented findings challenge the notion that cortical gamma oscillations can be entrained by rhythmic visual stimulation. Instead, the mechanism generating endogenous gamma oscillations seems to be resilient to external perturbation.
We aimed to investigate to what extent ongoing, high-frequency oscillations in the gamma-band (30-100 Hz) in the human brain can be entrained by a visual flicker. Gamma oscillations have long been suggested to coordinate neuronal firing and enable interregional communication. Our results demonstrate that rhythmic visual stimulation cannot hijack the dynamics of ongoing gamma oscillations; rather, the flicker response and the endogenous gamma oscillations coexist in different visual areas. Therefore, while a visual flicker evokes a strong neuronal response even at high frequencies in the gamma-band, it does not entrain endogenous gamma oscillations in visual cortex. This has important implications for interpreting studies investigating the causal and neuroprotective effects of rhythmic sensory stimulation in the gamma-band.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>34230106</pmid><doi>10.1523/JNEUROSCI.3134-20.2021</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-7887-3395</orcidid><orcidid>https://orcid.org/0000-0003-0323-2272</orcidid><orcidid>https://orcid.org/0000-0001-8193-8348</orcidid><orcidid>https://orcid.org/0000-0002-0934-418X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Biological Clocks - physiology Brain Brain Mapping - methods Cognitive science Entrainment Female Flicker Gamma Rhythm - physiology Humans Magnetoencephalography Magnetoencephalography - methods Male Oscillations Perturbation Photic Stimulation Rhythms Stimulation Visual cortex Visual Cortex - physiology Visual Perception - physiology Visual stimuli |
title | No Evidence for Entrainment: Endogenous Gamma Oscillations and Rhythmic Flicker Responses Coexist in Visual Cortex |
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