Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas

Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtaine...

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Published in	Neuron (Cambridge, Mass.) Vol. 89; no. 2; pp. 384 - 397
Main Authors	Michalareas, Georgios, Vezoli, Julien, van Pelt, Stan, Schoffelen, Jan-Mathijs, Kennedy, Henry, Fries, Pascal
Format	Journal Article
Language	English
Published	United States Elsevier Inc 20.01.2016 Elsevier Limited
Subjects	Alpha Rhythm - physiology Animals Beta Rhythm - physiology Bias Feedback Feedback, Physiological - physiology Female Gamma Rhythm - physiology Human subjects Humans Investigations Macaca Male Sensors Visual Cortex - physiology Visual Pathways - physiology Visual Perception - physiology
Online Access	Get full text
ISSN	0896-6273 1097-4199 1097-4199
DOI	10.1016/j.neuron.2015.12.018

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Abstract	Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtained in human subjects, we selected seven homologous macaque and human visual areas, and we correlated the macaque laminar projection patterns to human inter-areal directed influences as measured with magnetoencephalography. We show that influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. Rhythmic inter-areal influences constrain a functional hierarchy of the seven homologous human visual areas that is in close agreement with the respective macaque anatomical hierarchy. Rhythmic influences allow an extension of the hierarchy to 26 human visual areas including uniquely human brain areas. Hierarchical levels of ventral- and dorsal-stream visual areas are differentially affected by inter-areal influences in the alpha-beta band. •Gamma mediates forward and alpha-beta feedback influences among human visual areas•Human inter-areal directed influences correlate with macaque laminar connectivity•Rhythmic inter-areal influences establish a hierarchy of 26 human visual areas•Alpha-beta influences differentially affect ventral- and dorsal-stream visual areas Michalareas et al. show that in human visual cortex influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. These influences constrain a functional hierarchy in agreement with macaque anatomical hierarchy.
AbstractList	Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtained in human subjects, we selected seven homologous macaque and human visual areas, and we correlated the macaque laminar projection patterns to human inter-areal directed influences as measured with magnetoencephalography. We show that influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. Rhythmic inter-areal influences constrain a functional hierarchy of the seven homologous human visual areas that is in close agreement with the respective macaque anatomical hierarchy. Rhythmic influences allow an extension of the hierarchy to 26 human visual areas including uniquely human brain areas. Hierarchical levels of ventral- and dorsal-stream visual areas are differentially affected by inter-areal influences in the alpha-beta band.Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtained in human subjects, we selected seven homologous macaque and human visual areas, and we correlated the macaque laminar projection patterns to human inter-areal directed influences as measured with magnetoencephalography. We show that influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. Rhythmic inter-areal influences constrain a functional hierarchy of the seven homologous human visual areas that is in close agreement with the respective macaque anatomical hierarchy. Rhythmic influences allow an extension of the hierarchy to 26 human visual areas including uniquely human brain areas. Hierarchical levels of ventral- and dorsal-stream visual areas are differentially affected by inter-areal influences in the alpha-beta band. Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtained in human subjects, we selected seven homologous macaque and human visual areas, and correlated the macaque laminar projection patterns to human inter-areal directed influences as measured with magnetoencephalography. We show that influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. Rhythmic inter-areal influences constrain a functional hierarchy of the seven homologous human visual areas that is in close agreement with the respective macaque anatomical hierarchy. Rhythmic influences allow an extension of the hierarchy to 26 human visual areas including uniquely human brain areas. Hierarchical levels of ventral and dorsal stream visual areas are differentially affected by inter-areal influences in the alpha-beta band. Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtained in human subjects, we selected seven homologous macaque and human visual areas, and we correlated the macaque laminar projection patterns to human inter-areal directed influences as measured with magnetoencephalography. We show that influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. Rhythmic inter-areal influences constrain a functional hierarchy of the seven homologous human visual areas that is in close agreement with the respective macaque anatomical hierarchy. Rhythmic influences allow an extension of the hierarchy to 26 human visual areas including uniquely human brain areas. Hierarchical levels of ventral- and dorsal-stream visual areas are differentially affected by inter-areal influences in the alpha-beta band. •Gamma mediates forward and alpha-beta feedback influences among human visual areas•Human inter-areal directed influences correlate with macaque laminar connectivity•Rhythmic inter-areal influences establish a hierarchy of 26 human visual areas•Alpha-beta influences differentially affect ventral- and dorsal-stream visual areas Michalareas et al. show that in human visual cortex influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. These influences constrain a functional hierarchy in agreement with macaque anatomical hierarchy. Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtained in human subjects, we selected seven homologous macaque and human visual areas, and we correlated the macaque laminar projection patterns to human inter-areal directed influences as measured with magnetoencephalography. We show that influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. Rhythmic inter-areal influences constrain a functional hierarchy of the seven homologous human visual areas that is in close agreement with the respective macaque anatomical hierarchy. Rhythmic influences allow an extension of the hierarchy to 26 human visual areas including uniquely human brain areas. Hierarchical levels of ventral- and dorsal-stream visual areas are differentially affected by inter-areal influences in the alpha-beta band.
Author	Schoffelen, Jan-Mathijs Kennedy, Henry Michalareas, Georgios Fries, Pascal van Pelt, Stan Vezoli, Julien
AuthorAffiliation	2 Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Kapittelweg 29, 6525 EN Nijmegen, Netherlands 1 Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Deutschordenstraße 46, 60528 Frankfurt, Germany 3 Max Planck Institute for Psycholinguistics, Wundtlaan 1, 6525 XD Nijmegen, Netherlands 4 Stem Cell and Brain Research Institute, INSERM U846, 18 avenue Doyen Lépine, 69675 Bron, France 5 Université de Lyon, 37 rue du Repos, 69361 Lyon, France
AuthorAffiliation_xml	– name: 3 Max Planck Institute for Psycholinguistics, Wundtlaan 1, 6525 XD Nijmegen, Netherlands – name: 2 Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Kapittelweg 29, 6525 EN Nijmegen, Netherlands – name: 1 Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Deutschordenstraße 46, 60528 Frankfurt, Germany – name: 5 Université de Lyon, 37 rue du Repos, 69361 Lyon, France – name: 4 Stem Cell and Brain Research Institute, INSERM U846, 18 avenue Doyen Lépine, 69675 Bron, France
Author_xml	– sequence: 1 givenname: Georgios surname: Michalareas fullname: Michalareas, Georgios email: giorgos.michalareas@esi-frankfurt.de organization: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Deutschordenstraße 46, 60528 Frankfurt, Germany – sequence: 2 givenname: Julien surname: Vezoli fullname: Vezoli, Julien organization: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Deutschordenstraße 46, 60528 Frankfurt, Germany – sequence: 3 givenname: Stan surname: van Pelt fullname: van Pelt, Stan organization: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Deutschordenstraße 46, 60528 Frankfurt, Germany – sequence: 4 givenname: Jan-Mathijs surname: Schoffelen fullname: Schoffelen, Jan-Mathijs organization: Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Kapittelweg 29, 6525 EN Nijmegen, the Netherlands – sequence: 5 givenname: Henry surname: Kennedy fullname: Kennedy, Henry organization: Stem Cell and Brain Research Institute, INSERM U846, 18 Avenue Doyen Lépine, 69675 Bron, France – sequence: 6 givenname: Pascal surname: Fries fullname: Fries, Pascal email: pascal.fries@esi-frankfurt.de organization: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Deutschordenstraße 46, 60528 Frankfurt, Germany
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26777277$$D View this record in MEDLINE/PubMed
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Snippet	Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed...
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SubjectTerms	Alpha Rhythm - physiology Animals Beta Rhythm - physiology Bias Feedback Feedback, Physiological - physiology Female Gamma Rhythm - physiology Human subjects Humans Investigations Macaca Male Sensors Visual Cortex - physiology Visual Pathways - physiology Visual Perception - physiology
Title	Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas
URI	https://dx.doi.org/10.1016/j.neuron.2015.12.018 https://www.ncbi.nlm.nih.gov/pubmed/26777277 https://www.proquest.com/docview/1759011009 https://www.proquest.com/docview/1790022922 https://pubmed.ncbi.nlm.nih.gov/PMC4871751
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