Medication‐invariant resting aperiodic and periodic neural activity in Parkinson's disease
Parkinson's disease (PD) has been associated with greater total power in canonical frequency bands (i.e., alpha, beta) of the resting electroencephalogram (EEG). However, PD has also been associated with a reduction in the proportion of total power across all frequency bands. This discrepancy m...
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description | Parkinson's disease (PD) has been associated with greater total power in canonical frequency bands (i.e., alpha, beta) of the resting electroencephalogram (EEG). However, PD has also been associated with a reduction in the proportion of total power across all frequency bands. This discrepancy may be explained by aperiodic activity (exponent and offset) present across all frequency bands. Here, we examined differences in the eyes‐open (EO) and eyes‐closed (EC) resting EEG of PD participants (N = 26) on and off medication, and age‐matched healthy controls (CTL; N = 26). We extracted power from canonical frequency bands using traditional methods (total alpha and beta power) and extracted separate parameters for periodic (parameterized alpha and beta power) and aperiodic activity (exponent and offset). Cluster‐based permutation tests over spatial and frequency dimensions indicated that total alpha and beta power, and aperiodic exponent and offset were greater in PD participants, independent of medication status. After removing the exponent and offset, greater alpha power in PD (vs. CTL) was only present in EO recordings and no reliable differences in beta power were observed. Differences between PD and CTL in the resting EEG are likely driven by aperiodic activity, suggestive of greater relative inhibitory neural activity and greater neuronal spiking. Our findings suggest that resting EEG activity in PD is characterized by medication‐invariant differences in aperiodic activity which is independent of the increase in alpha power with EO. This highlights the importance of considering aperiodic activity contributions to the neural correlates of brain disorders.
Parkinson's disease (PD) is marked not only by greater total power in alpha and beta frequency bands of EEG but also with a reduction in total power potentially due to changes in aperiodic activity. We provide evidence that a greater exponent and offset (greater inhibition) in aperiodic activity drive frequency band changes in PD. Furthermore, we demonstrate the efficacy of EEG as a non‐invasive technique to assess changes in excitation and inhibition (E:I) balance and PD biomarkers. |
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Parkinson's disease (PD) is marked not only by greater total power in alpha and beta frequency bands of EEG but also with a reduction in total power potentially due to changes in aperiodic activity. We provide evidence that a greater exponent and offset (greater inhibition) in aperiodic activity drive frequency band changes in PD. Furthermore, we demonstrate the efficacy of EEG as a non‐invasive technique to assess changes in excitation and inhibition (E:I) balance and PD biomarkers.</description><identifier>ISSN: 0048-5772</identifier><identifier>ISSN: 1469-8986</identifier><identifier>EISSN: 1469-8986</identifier><identifier>EISSN: 1540-5958</identifier><identifier>DOI: 10.1111/psyp.14478</identifier><identifier>PMID: 37937898</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>aperiodic activity ; cluster‐based permutation tests ; Cytotoxicity ; EEG ; Electroencephalography ; excitatory and inhibitory (E:I) balance ; Firing pattern ; Frequency dependence ; Humans ; Lymphocytes T ; Movement disorders ; Neurodegenerative diseases ; Parkinson Disease ; Parkinson's disease ; Rest - physiology</subject><ispartof>Psychophysiology, 2024-04, Vol.61 (4), p.e14478-n/a</ispartof><rights>2023 The Authors. published by Wiley Periodicals LLC on behalf of Society for Psychophysiological Research.</rights><rights>2023 The Authors. Psychophysiology published by Wiley Periodicals LLC on behalf of Society for Psychophysiological Research.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c4088-65c4902987860195c2166adc97b1beeb8d7fe9cdc6a46fe3cf35b316220db66b3</cites><orcidid>0000-0001-5971-273X ; 0000-0002-0881-9147 ; 0000-0002-2345-2806 ; 0000-0003-3976-5855 ; 0000-0003-0298-6806 ; 0000-0003-2428-3562 ; 0000-0001-9722-2475 ; 0000-0003-2256-0597</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fpsyp.14478$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpsyp.14478$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,778,782,883,1414,27907,27908,45557,45558</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37937898$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>McKeown, Daniel J.</creatorcontrib><creatorcontrib>Jones, Manon</creatorcontrib><creatorcontrib>Pihl, Camilla</creatorcontrib><creatorcontrib>Finley, Anna J.</creatorcontrib><creatorcontrib>Kelley, Nicholas</creatorcontrib><creatorcontrib>Baumann, Oliver</creatorcontrib><creatorcontrib>Schinazi, Victor R.</creatorcontrib><creatorcontrib>Moustafa, Ahmed A.</creatorcontrib><creatorcontrib>Cavanagh, James F.</creatorcontrib><creatorcontrib>Angus, Douglas J.</creatorcontrib><title>Medication‐invariant resting aperiodic and periodic neural activity in Parkinson's disease</title><title>Psychophysiology</title><addtitle>Psychophysiology</addtitle><description>Parkinson's disease (PD) has been associated with greater total power in canonical frequency bands (i.e., alpha, beta) of the resting electroencephalogram (EEG). However, PD has also been associated with a reduction in the proportion of total power across all frequency bands. This discrepancy may be explained by aperiodic activity (exponent and offset) present across all frequency bands. Here, we examined differences in the eyes‐open (EO) and eyes‐closed (EC) resting EEG of PD participants (N = 26) on and off medication, and age‐matched healthy controls (CTL; N = 26). We extracted power from canonical frequency bands using traditional methods (total alpha and beta power) and extracted separate parameters for periodic (parameterized alpha and beta power) and aperiodic activity (exponent and offset). Cluster‐based permutation tests over spatial and frequency dimensions indicated that total alpha and beta power, and aperiodic exponent and offset were greater in PD participants, independent of medication status. After removing the exponent and offset, greater alpha power in PD (vs. CTL) was only present in EO recordings and no reliable differences in beta power were observed. Differences between PD and CTL in the resting EEG are likely driven by aperiodic activity, suggestive of greater relative inhibitory neural activity and greater neuronal spiking. Our findings suggest that resting EEG activity in PD is characterized by medication‐invariant differences in aperiodic activity which is independent of the increase in alpha power with EO. This highlights the importance of considering aperiodic activity contributions to the neural correlates of brain disorders.
Parkinson's disease (PD) is marked not only by greater total power in alpha and beta frequency bands of EEG but also with a reduction in total power potentially due to changes in aperiodic activity. We provide evidence that a greater exponent and offset (greater inhibition) in aperiodic activity drive frequency band changes in PD. Furthermore, we demonstrate the efficacy of EEG as a non‐invasive technique to assess changes in excitation and inhibition (E:I) balance and PD biomarkers.</description><subject>aperiodic activity</subject><subject>cluster‐based permutation tests</subject><subject>Cytotoxicity</subject><subject>EEG</subject><subject>Electroencephalography</subject><subject>excitatory and inhibitory (E:I) balance</subject><subject>Firing pattern</subject><subject>Frequency dependence</subject><subject>Humans</subject><subject>Lymphocytes T</subject><subject>Movement disorders</subject><subject>Neurodegenerative diseases</subject><subject>Parkinson Disease</subject><subject>Parkinson's disease</subject><subject>Rest - physiology</subject><issn>0048-5772</issn><issn>1469-8986</issn><issn>1469-8986</issn><issn>1540-5958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp9kd1qFDEYhoModrt60guQAQ8qwtQkk8nPkZSirdDSBfVAKIRM5puaOpuMycyWPfMSeo1eSdNuu6gH5iSEPDy83_citEfwAcnn3ZDWwwFhTMgnaEYYV6VUkj9FM4yZLGsh6A7aTekKY6wIpc_RTiVUJTI0Qxdn0DprRhf87183zq9MdMaPRYQ0On9ZmAGiCxkpjG-L7cPDFE1fGDu6lRvXhfPFwsQfzqfg91PRugQmwQv0rDN9gpcP9xx9_fjhy9FJeXp-_Ono8LS0DEtZ8toyhamSQnJMVG0p4dy0VomGNACNbEUHyraWG8Y7qGxX1U1FOKW4bThvqjl6v_EOU7OE1oIfczo9RLc0ca2DcfrvH---68uw0oTUjBJRZcObB0MMP6c8u166ZKHvjYcwJU2lFEzUKu9tjl7_g16FKfo8n6aq5ljwWvJMvd1QNoaUInTbNATru9b0XWv6vrUMv_oz_xZ9rCkDZANcux7W_1Hpxedvi430FhnxpeU</recordid><startdate>202404</startdate><enddate>202404</enddate><creator>McKeown, Daniel J.</creator><creator>Jones, Manon</creator><creator>Pihl, Camilla</creator><creator>Finley, Anna J.</creator><creator>Kelley, Nicholas</creator><creator>Baumann, Oliver</creator><creator>Schinazi, Victor R.</creator><creator>Moustafa, Ahmed A.</creator><creator>Cavanagh, James F.</creator><creator>Angus, Douglas J.</creator><general>Blackwell Publishing Ltd</general><scope>24P</scope><scope>WIN</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>7TK</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5971-273X</orcidid><orcidid>https://orcid.org/0000-0002-0881-9147</orcidid><orcidid>https://orcid.org/0000-0002-2345-2806</orcidid><orcidid>https://orcid.org/0000-0003-3976-5855</orcidid><orcidid>https://orcid.org/0000-0003-0298-6806</orcidid><orcidid>https://orcid.org/0000-0003-2428-3562</orcidid><orcidid>https://orcid.org/0000-0001-9722-2475</orcidid><orcidid>https://orcid.org/0000-0003-2256-0597</orcidid></search><sort><creationdate>202404</creationdate><title>Medication‐invariant resting aperiodic and periodic neural activity in Parkinson's disease</title><author>McKeown, Daniel J. ; Jones, Manon ; Pihl, Camilla ; Finley, Anna J. ; Kelley, Nicholas ; Baumann, Oliver ; Schinazi, Victor R. ; Moustafa, Ahmed A. ; Cavanagh, James F. ; Angus, Douglas J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4088-65c4902987860195c2166adc97b1beeb8d7fe9cdc6a46fe3cf35b316220db66b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>aperiodic activity</topic><topic>cluster‐based permutation tests</topic><topic>Cytotoxicity</topic><topic>EEG</topic><topic>Electroencephalography</topic><topic>excitatory and inhibitory (E:I) balance</topic><topic>Firing pattern</topic><topic>Frequency dependence</topic><topic>Humans</topic><topic>Lymphocytes T</topic><topic>Movement disorders</topic><topic>Neurodegenerative diseases</topic><topic>Parkinson Disease</topic><topic>Parkinson's disease</topic><topic>Rest - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>McKeown, Daniel J.</creatorcontrib><creatorcontrib>Jones, Manon</creatorcontrib><creatorcontrib>Pihl, Camilla</creatorcontrib><creatorcontrib>Finley, Anna J.</creatorcontrib><creatorcontrib>Kelley, Nicholas</creatorcontrib><creatorcontrib>Baumann, Oliver</creatorcontrib><creatorcontrib>Schinazi, Victor R.</creatorcontrib><creatorcontrib>Moustafa, Ahmed A.</creatorcontrib><creatorcontrib>Cavanagh, James F.</creatorcontrib><creatorcontrib>Angus, Douglas J.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Psychophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>McKeown, Daniel J.</au><au>Jones, Manon</au><au>Pihl, Camilla</au><au>Finley, Anna J.</au><au>Kelley, Nicholas</au><au>Baumann, Oliver</au><au>Schinazi, Victor R.</au><au>Moustafa, Ahmed A.</au><au>Cavanagh, James F.</au><au>Angus, Douglas J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Medication‐invariant resting aperiodic and periodic neural activity in Parkinson's disease</atitle><jtitle>Psychophysiology</jtitle><addtitle>Psychophysiology</addtitle><date>2024-04</date><risdate>2024</risdate><volume>61</volume><issue>4</issue><spage>e14478</spage><epage>n/a</epage><pages>e14478-n/a</pages><issn>0048-5772</issn><issn>1469-8986</issn><eissn>1469-8986</eissn><eissn>1540-5958</eissn><abstract>Parkinson's disease (PD) has been associated with greater total power in canonical frequency bands (i.e., alpha, beta) of the resting electroencephalogram (EEG). However, PD has also been associated with a reduction in the proportion of total power across all frequency bands. This discrepancy may be explained by aperiodic activity (exponent and offset) present across all frequency bands. Here, we examined differences in the eyes‐open (EO) and eyes‐closed (EC) resting EEG of PD participants (N = 26) on and off medication, and age‐matched healthy controls (CTL; N = 26). We extracted power from canonical frequency bands using traditional methods (total alpha and beta power) and extracted separate parameters for periodic (parameterized alpha and beta power) and aperiodic activity (exponent and offset). Cluster‐based permutation tests over spatial and frequency dimensions indicated that total alpha and beta power, and aperiodic exponent and offset were greater in PD participants, independent of medication status. After removing the exponent and offset, greater alpha power in PD (vs. CTL) was only present in EO recordings and no reliable differences in beta power were observed. Differences between PD and CTL in the resting EEG are likely driven by aperiodic activity, suggestive of greater relative inhibitory neural activity and greater neuronal spiking. Our findings suggest that resting EEG activity in PD is characterized by medication‐invariant differences in aperiodic activity which is independent of the increase in alpha power with EO. This highlights the importance of considering aperiodic activity contributions to the neural correlates of brain disorders.
Parkinson's disease (PD) is marked not only by greater total power in alpha and beta frequency bands of EEG but also with a reduction in total power potentially due to changes in aperiodic activity. We provide evidence that a greater exponent and offset (greater inhibition) in aperiodic activity drive frequency band changes in PD. Furthermore, we demonstrate the efficacy of EEG as a non‐invasive technique to assess changes in excitation and inhibition (E:I) balance and PD biomarkers.</abstract><cop>United States</cop><pub>Blackwell Publishing Ltd</pub><pmid>37937898</pmid><doi>10.1111/psyp.14478</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-5971-273X</orcidid><orcidid>https://orcid.org/0000-0002-0881-9147</orcidid><orcidid>https://orcid.org/0000-0002-2345-2806</orcidid><orcidid>https://orcid.org/0000-0003-3976-5855</orcidid><orcidid>https://orcid.org/0000-0003-0298-6806</orcidid><orcidid>https://orcid.org/0000-0003-2428-3562</orcidid><orcidid>https://orcid.org/0000-0001-9722-2475</orcidid><orcidid>https://orcid.org/0000-0003-2256-0597</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | aperiodic activity cluster‐based permutation tests Cytotoxicity EEG Electroencephalography excitatory and inhibitory (E:I) balance Firing pattern Frequency dependence Humans Lymphocytes T Movement disorders Neurodegenerative diseases Parkinson Disease Parkinson's disease Rest - physiology |
title | Medication‐invariant resting aperiodic and periodic neural activity in Parkinson's disease |
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