Structural basis of envelope and phase intrinsic coupling modes in the cerebral cortex
Arnaud Messé,
Karl J. Hollensteiner,
Céline Delettre,
Leigh-Anne Dell-Brown,
Florian Pieper,
Lena J. Nentwig,
Edgar E. Galindo-Leon,
Benoît Larrat,
Sébastien Mériaux,
Jean-François Mangin,
Isabel Reillo,
Camino de Juan Romero,
Víctor Borrell,
Gerhard Engler,
Roberto Toro,
Andreas K. Engel,
Claus C. Hilgetag
Affiliations
Arnaud Messé
Corresponding author.; Institute of Computational Neuroscience, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany
Karl J. Hollensteiner
Department of Neurophysiology and Pathophysiology, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany
Céline Delettre
Institute of Computational Neuroscience, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany; Unité de Neuroanatomie Appliquée et Théorique, Unité de Génétique Humaine et Fonctions Cognitives, Institut Pasteur, Université Paris Cité, 25-28 rue du Dr Roux, Paris 75015, France
Leigh-Anne Dell-Brown
Institute of Computational Neuroscience, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany
Florian Pieper
Department of Neurophysiology and Pathophysiology, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany
Lena J. Nentwig
Institute of Computational Neuroscience, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany
Edgar E. Galindo-Leon
Department of Neurophysiology and Pathophysiology, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany
Benoît Larrat
NeuroSpin, CEA, Paris-Saclay University, Centre d’études de Saclay, Bâtiment 145, Gif-sur-Yvette 91191, France
Sébastien Mériaux
NeuroSpin, CEA, Paris-Saclay University, Centre d’études de Saclay, Bâtiment 145, Gif-sur-Yvette 91191, France
Jean-François Mangin
NeuroSpin, CEA, Paris-Saclay University, Centre d’études de Saclay, Bâtiment 145, Gif-sur-Yvette 91191, France
Isabel Reillo
Developmental Neurobiology Unit, Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas - Universidad Miguel Hernández, Sant Joan d’Alacant, Av. Santiago Ramón y Cajal s/n, Sant Joan d’Alacant 03550, Spain
Camino de Juan Romero
Developmental Neurobiology Unit, Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas - Universidad Miguel Hernández, Sant Joan d’Alacant, Av. Santiago Ramón y Cajal s/n, Sant Joan d’Alacant 03550, Spain
Víctor Borrell
Developmental Neurobiology Unit, Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas - Universidad Miguel Hernández, Sant Joan d’Alacant, Av. Santiago Ramón y Cajal s/n, Sant Joan d’Alacant 03550, Spain
Gerhard Engler
Department of Neurophysiology and Pathophysiology, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany
Roberto Toro
Unité de Neuroanatomie Appliquée et Théorique, Unité de Génétique Humaine et Fonctions Cognitives, Institut Pasteur, Université Paris Cité, 25-28 rue du Dr Roux, Paris 75015, France; Center for Research and Interdisciplinarity, Paris Descartes University, 24, rue du Faubourg Saint Jacques, Paris 75014, France
Andreas K. Engel
Department of Neurophysiology and Pathophysiology, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany
Claus C. Hilgetag
Institute of Computational Neuroscience, Hamburg Center of Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Martinistraße 52, Hamburg 20246, Germany; Department of Health Sciences, Boston University, 635 Commonwealth Avenue, Boston, Massachusetts 02215, USA
Intrinsic coupling modes (ICMs) can be observed in ongoing brain activity at multiple spatial and temporal scales. Two families of ICMs can be distinguished: phase and envelope ICMs. The principles that shape these ICMs remain partly elusive, in particular their relation to the underlying brain structure. Here we explored structure-function relationships in the ferret brain between ICMs quantified from ongoing brain activity recorded with chronically implanted micro-ECoG arrays and structural connectivity (SC) obtained from high-resolution diffusion MRI tractography. Large-scale computational models were used to explore the ability to predict both types of ICMs. Importantly, all investigations were conducted with ICM measures that are sensitive or insensitive to volume conduction effects. The results show that both types of ICMs are significantly related to SC, except for phase ICMs when using measures removing zero-lag coupling. The correlation between SC and ICMs increases with increasing frequency which is accompanied by reduced delays. Computational models produced results that were highly dependent on the specific parameter settings. The most consistent predictions were derived from measures solely based on SC. Overall, the results demonstrate that patterns of cortical functional coupling as reflected in both phase and envelope ICMs are both related, albeit to different degrees, to the underlying structural connectivity in the cerebral cortex.
