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Time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity during resting-state and respiratory challenges assessed by multimodal functional near-infrared spectroscopy
Monitoring respiratory processes is important for evaluating neuroimaging data, given their influence on time–frequency dynamics of intra- and extracerebral hemodynamics. Here we investigated the time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity state...
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Published in: | NeuroImage (Orlando, Fla.) Fla.), 2015-10, Vol.120, p.481-492 |
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description | Monitoring respiratory processes is important for evaluating neuroimaging data, given their influence on time–frequency dynamics of intra- and extracerebral hemodynamics. Here we investigated the time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity states during hypo- and hypercapnia by using three different respiratory challenge tasks (i.e., hyperventilation, breath-holding, and rebreathing) compared to resting-state. The sum of intra- and extracerebral hemodynamic responses were assessed using functional near-infrared spectroscopy (fNIRS) within two regions of interest (i.e., the dorsolateral and the medial prefrontal cortex). Time–frequency fNIRS analysis was performed based on wavelet transform coherence to quantify functional connectivity in terms of positive and negative phase-coupling within each region of interest. Physiological measures were assessed in the form of partial end-tidal carbon dioxide, heart rate, arterial tissue oxygen saturation, and respiration rate.
We found that the three respiration challenges modulated time–frequency dynamics differently with respect to resting-state: 1) Hyperventilation and breath-holding exhibited inverse patterns of positive and negative phase-coupling. 2) In contrast, rebreathing had no significant effect. 3) Low-frequency oscillations contributed to a greater extent to time–frequency dynamics compared to high-frequency oscillations.
The results highlight that there exist distinct differences in time–frequency dynamics of the sum of intra- and extracerebral functional connectivity not only between hypo- (hyperventilation) and hypercapnia but also between different states of hypercapnia (breath-holding versus rebreathing). This suggests that a multimodal assessment of intra-/extracerebral and systemic physiological changes during respiratory challenges compared to resting-state may have potential use in the differentiation between physiological and pathological respiratory behavior accompanied by the psycho-physiological state of a human.
•Hemodynamic changes were compared between hypo-/hypercapnia and resting-state.•Time–frequency dynamics were assessed using wavelet transform coherence.•Hyperventilation and breath-holding exhibited significant effects on phase-coupling.•Rebreathing had no effect on phase-coupling.•Results may support separating physio- from pathological respiratory behavior. |
doi_str_mv | 10.1016/j.neuroimage.2015.07.021 |
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We found that the three respiration challenges modulated time–frequency dynamics differently with respect to resting-state: 1) Hyperventilation and breath-holding exhibited inverse patterns of positive and negative phase-coupling. 2) In contrast, rebreathing had no significant effect. 3) Low-frequency oscillations contributed to a greater extent to time–frequency dynamics compared to high-frequency oscillations.
The results highlight that there exist distinct differences in time–frequency dynamics of the sum of intra- and extracerebral functional connectivity not only between hypo- (hyperventilation) and hypercapnia but also between different states of hypercapnia (breath-holding versus rebreathing). This suggests that a multimodal assessment of intra-/extracerebral and systemic physiological changes during respiratory challenges compared to resting-state may have potential use in the differentiation between physiological and pathological respiratory behavior accompanied by the psycho-physiological state of a human.
•Hemodynamic changes were compared between hypo-/hypercapnia and resting-state.•Time–frequency dynamics were assessed using wavelet transform coherence.•Hyperventilation and breath-holding exhibited significant effects on phase-coupling.•Rebreathing had no effect on phase-coupling.•Results may support separating physio- from pathological respiratory behavior.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2015.07.021</identifier><identifier>PMID: 26169319</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adult ; Anxiety ; Brain ; Breath Holding ; Capnography ; Carbon dioxide ; Female ; Functional near-infrared spectroscopy ; Functional Neuroimaging ; Hemodynamics - physiology ; Humans ; Hypercapnia - physiopathology ; Hyperventilation - physiopathology ; Hypocapnia - physiopathology ; Hypoventilation - physiopathology ; Male ; Neurovascular Coupling - physiology ; Partial pressure of carbon dioxide ; Physiology ; Prefrontal Cortex - physiology ; Prefrontal Cortex - physiopathology ; Respiration ; Resting-state ; Spectroscopy, Near-Infrared - methods ; Spectrum analysis ; Studies ; Time–frequency dynamics of intra- and extracortical hemodynamic functional connectivity ; Wavelet transforms</subject><ispartof>NeuroImage (Orlando, Fla.), 2015-10, Vol.120, p.481-492</ispartof><rights>2015 Elsevier Inc.</rights><rights>Copyright © 2015 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Oct 15, 2015</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c435t-4b1b921de9aea532b1358f71b76477f7da526a41ddbaebc660a7ea3b74117df63</citedby><cites>FETCH-LOGICAL-c435t-4b1b921de9aea532b1358f71b76477f7da526a41ddbaebc660a7ea3b74117df63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26169319$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Holper, L.</creatorcontrib><creatorcontrib>Scholkmann, F.</creatorcontrib><creatorcontrib>Seifritz, E.</creatorcontrib><title>Time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity during resting-state and respiratory challenges assessed by multimodal functional near-infrared spectroscopy</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>Monitoring respiratory processes is important for evaluating neuroimaging data, given their influence on time–frequency dynamics of intra- and extracerebral hemodynamics. Here we investigated the time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity states during hypo- and hypercapnia by using three different respiratory challenge tasks (i.e., hyperventilation, breath-holding, and rebreathing) compared to resting-state. The sum of intra- and extracerebral hemodynamic responses were assessed using functional near-infrared spectroscopy (fNIRS) within two regions of interest (i.e., the dorsolateral and the medial prefrontal cortex). Time–frequency fNIRS analysis was performed based on wavelet transform coherence to quantify functional connectivity in terms of positive and negative phase-coupling within each region of interest. Physiological measures were assessed in the form of partial end-tidal carbon dioxide, heart rate, arterial tissue oxygen saturation, and respiration rate.
We found that the three respiration challenges modulated time–frequency dynamics differently with respect to resting-state: 1) Hyperventilation and breath-holding exhibited inverse patterns of positive and negative phase-coupling. 2) In contrast, rebreathing had no significant effect. 3) Low-frequency oscillations contributed to a greater extent to time–frequency dynamics compared to high-frequency oscillations.
The results highlight that there exist distinct differences in time–frequency dynamics of the sum of intra- and extracerebral functional connectivity not only between hypo- (hyperventilation) and hypercapnia but also between different states of hypercapnia (breath-holding versus rebreathing). This suggests that a multimodal assessment of intra-/extracerebral and systemic physiological changes during respiratory challenges compared to resting-state may have potential use in the differentiation between physiological and pathological respiratory behavior accompanied by the psycho-physiological state of a human.
•Hemodynamic changes were compared between hypo-/hypercapnia and resting-state.•Time–frequency dynamics were assessed using wavelet transform coherence.•Hyperventilation and breath-holding exhibited significant effects on phase-coupling.•Rebreathing had no effect on phase-coupling.•Results may support separating physio- from pathological respiratory behavior.</description><subject>Adult</subject><subject>Anxiety</subject><subject>Brain</subject><subject>Breath Holding</subject><subject>Capnography</subject><subject>Carbon dioxide</subject><subject>Female</subject><subject>Functional near-infrared spectroscopy</subject><subject>Functional Neuroimaging</subject><subject>Hemodynamics - physiology</subject><subject>Humans</subject><subject>Hypercapnia - physiopathology</subject><subject>Hyperventilation - physiopathology</subject><subject>Hypocapnia - physiopathology</subject><subject>Hypoventilation - physiopathology</subject><subject>Male</subject><subject>Neurovascular Coupling - physiology</subject><subject>Partial pressure of carbon dioxide</subject><subject>Physiology</subject><subject>Prefrontal Cortex - physiology</subject><subject>Prefrontal Cortex - physiopathology</subject><subject>Respiration</subject><subject>Resting-state</subject><subject>Spectroscopy, Near-Infrared - methods</subject><subject>Spectrum analysis</subject><subject>Studies</subject><subject>Time–frequency dynamics of intra- and extracortical hemodynamic functional connectivity</subject><subject>Wavelet transforms</subject><issn>1053-8119</issn><issn>1095-9572</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNqNkkuO1DAQhiMEYoaBKyBLbNgkuPJysoQRL2kkNsPacuxKt1uJ3djOiOzmDpyMK8xJpppuHmIDkqUqW1_9v1z6s4wBL4BD-2pXOFyCt7PaYFFyaAouCl7Cg-wceN_kfSPKh4e-qfIOoD_LnsS445z3UHePs7OyhbavoD_Pvl_bGe9uv40Bvyzo9MrM6tRsdWR-ZGmLLC7zobUuBZUz5QzDr9RqDDgENbEtzv40w8bF6WS9o2ftnUO63NhEmkuwbsMCxkQ1j0kl_CFFL3sbVPJhZXqrpgndBiNTMSIdw4aVzcuULFmQ5h_yDlXIrRuDCoTFPVkFH7Xfr0-zR6OaIj471Yvs87u315cf8qtP7z9evr7KdV01Ka8HGPoSDPYKVVOVA1RNNwoYRFsLMQqjmrJVNRgzKBx023IlUFWDqAGEGdvqInt51N0HT6uLSc42apwm5dAvUYJooIS6huY_UOg4-bYVoS_-Qnd-CfRjorqOV6IDfqC6I6Xp0zHgKPeBwhBWCVweEiJ38ndC5CEhkgtJCaHR5yeDZZjR_Br8GQkC3hwBpOXdWAwyakvJQGMDbVkab__tcg8EXNnz</recordid><startdate>20151015</startdate><enddate>20151015</enddate><creator>Holper, L.</creator><creator>Scholkmann, F.</creator><creator>Seifritz, E.</creator><general>Elsevier Inc</general><general>Elsevier Limited</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>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>7QO</scope></search><sort><creationdate>20151015</creationdate><title>Time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity during resting-state and respiratory challenges assessed by multimodal functional near-infrared spectroscopy</title><author>Holper, L. ; Scholkmann, F. ; Seifritz, E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c435t-4b1b921de9aea532b1358f71b76477f7da526a41ddbaebc660a7ea3b74117df63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adult</topic><topic>Anxiety</topic><topic>Brain</topic><topic>Breath Holding</topic><topic>Capnography</topic><topic>Carbon dioxide</topic><topic>Female</topic><topic>Functional near-infrared spectroscopy</topic><topic>Functional Neuroimaging</topic><topic>Hemodynamics - physiology</topic><topic>Humans</topic><topic>Hypercapnia - physiopathology</topic><topic>Hyperventilation - physiopathology</topic><topic>Hypocapnia - physiopathology</topic><topic>Hypoventilation - physiopathology</topic><topic>Male</topic><topic>Neurovascular Coupling - physiology</topic><topic>Partial pressure of carbon dioxide</topic><topic>Physiology</topic><topic>Prefrontal Cortex - physiology</topic><topic>Prefrontal Cortex - physiopathology</topic><topic>Respiration</topic><topic>Resting-state</topic><topic>Spectroscopy, Near-Infrared - methods</topic><topic>Spectrum analysis</topic><topic>Studies</topic><topic>Time–frequency dynamics of intra- and extracortical hemodynamic functional connectivity</topic><topic>Wavelet transforms</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Holper, L.</creatorcontrib><creatorcontrib>Scholkmann, F.</creatorcontrib><creatorcontrib>Seifritz, 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>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database (ProQuest)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Biotechnology Research Abstracts</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Holper, L.</au><au>Scholkmann, F.</au><au>Seifritz, E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity during resting-state and respiratory challenges assessed by multimodal functional near-infrared spectroscopy</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2015-10-15</date><risdate>2015</risdate><volume>120</volume><spage>481</spage><epage>492</epage><pages>481-492</pages><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>Monitoring respiratory processes is important for evaluating neuroimaging data, given their influence on time–frequency dynamics of intra- and extracerebral hemodynamics. Here we investigated the time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity states during hypo- and hypercapnia by using three different respiratory challenge tasks (i.e., hyperventilation, breath-holding, and rebreathing) compared to resting-state. The sum of intra- and extracerebral hemodynamic responses were assessed using functional near-infrared spectroscopy (fNIRS) within two regions of interest (i.e., the dorsolateral and the medial prefrontal cortex). Time–frequency fNIRS analysis was performed based on wavelet transform coherence to quantify functional connectivity in terms of positive and negative phase-coupling within each region of interest. Physiological measures were assessed in the form of partial end-tidal carbon dioxide, heart rate, arterial tissue oxygen saturation, and respiration rate.
We found that the three respiration challenges modulated time–frequency dynamics differently with respect to resting-state: 1) Hyperventilation and breath-holding exhibited inverse patterns of positive and negative phase-coupling. 2) In contrast, rebreathing had no significant effect. 3) Low-frequency oscillations contributed to a greater extent to time–frequency dynamics compared to high-frequency oscillations.
The results highlight that there exist distinct differences in time–frequency dynamics of the sum of intra- and extracerebral functional connectivity not only between hypo- (hyperventilation) and hypercapnia but also between different states of hypercapnia (breath-holding versus rebreathing). This suggests that a multimodal assessment of intra-/extracerebral and systemic physiological changes during respiratory challenges compared to resting-state may have potential use in the differentiation between physiological and pathological respiratory behavior accompanied by the psycho-physiological state of a human.
•Hemodynamic changes were compared between hypo-/hypercapnia and resting-state.•Time–frequency dynamics were assessed using wavelet transform coherence.•Hyperventilation and breath-holding exhibited significant effects on phase-coupling.•Rebreathing had no effect on phase-coupling.•Results may support separating physio- from pathological respiratory behavior.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>26169319</pmid><doi>10.1016/j.neuroimage.2015.07.021</doi><tpages>12</tpages></addata></record> |
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subjects | Adult Anxiety Brain Breath Holding Capnography Carbon dioxide Female Functional near-infrared spectroscopy Functional Neuroimaging Hemodynamics - physiology Humans Hypercapnia - physiopathology Hyperventilation - physiopathology Hypocapnia - physiopathology Hypoventilation - physiopathology Male Neurovascular Coupling - physiology Partial pressure of carbon dioxide Physiology Prefrontal Cortex - physiology Prefrontal Cortex - physiopathology Respiration Resting-state Spectroscopy, Near-Infrared - methods Spectrum analysis Studies Time–frequency dynamics of intra- and extracortical hemodynamic functional connectivity Wavelet transforms |
title | Time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity during resting-state and respiratory challenges assessed by multimodal functional near-infrared spectroscopy |
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