Functional architecture of executive processes: Evidence from verbal fluency and lesion mapping in stroke patients

Olivier Godefroy; Ardalan Aarabi; Flore Dorchies; Mélanie Barbay; Daniela Andriuta; Momar Diouf; Michel Thiebaut de Schotten; Rania Kassir; Sophie Tasseel-Ponche; Martine Roussel; GRECogVASC study group

doi:10.1016/j.cortex.2023.03.013

Functional architecture of executive processes: Evidence from verbal fluency and lesion mapping in stroke patients

Cortex. 2023 Jul:164:129-143. doi: 10.1016/j.cortex.2023.03.013. Epub 2023 Apr 29.

Collaborators

GRECogVASC study group:
Olivier Godefroy⁸, Martine Roussel⁸, Mélanie Barbay⁸, Sandrine Canaple⁸, Chantal Lamy⁸, Claire Leclercq⁸, Audrey Courselle-Arnoux⁸, Sandrine Despretz-Wannepain⁹, Pascal Despretz¹⁰, Hassan Berrissoul¹¹, Carl Picard¹², Momar Diouf¹², Gwénolé Loas¹³, Hervé Deramond¹⁴, Hervé Taillia¹⁵, Anne-Emmanuelle Ardisson¹⁵, Claudine Nédélec-Ciceri¹⁶, Camille Bonnin¹⁶, Catherine Thomas-Anterion¹⁷, Francoise Vincent-Grangette¹⁸, Jérome Varvat¹⁷, Véronique Quaglino¹⁹, Hélène Beaunieux²⁰, Christine Moroni²¹, Audrey Martens-Chazelles²², Stéphanie Batier-Monperrus²³, Cécile Monteleone²⁴, Véronique Costantino²⁴, Eric Theunssens²⁵

Affiliations

¹ Laboratory of Functional Neurosciences (UR UPJV 4559), Jules Verne University of Picardie, Amiens, France; Departments of Neurology, Amiens University Hospital, France. Electronic address: [email protected].
² Laboratory of Functional Neurosciences (UR UPJV 4559), Jules Verne University of Picardie, Amiens, France.
³ Laboratory of Functional Neurosciences (UR UPJV 4559), Jules Verne University of Picardie, Amiens, France; Departments of Neurology, Amiens University Hospital, France.
⁴ Departments of Biostatistics, Amiens University Hospital, France.
⁵ Groupe d'Imagerie Neurofonctionnelle, Institut des Maladies Neurodégénératives-UMR 5293, CNRS, CEA, University of Bordeaux, Bordeaux, France; Brain Connectivity and Behaviour Laboratory, Sorbonne Universities, Paris, France.
⁶ Laboratory of Functional Neurosciences (UR UPJV 4559), Jules Verne University of Picardie, Amiens, France; Laboratoire de Recherche en Neurosciences (LAREN), Université Saint-Joseph, Beyrouth, Lebanon.
⁷ Laboratory of Functional Neurosciences (UR UPJV 4559), Jules Verne University of Picardie, Amiens, France; Departments of Physical Medicine and Rehabilitation, Amiens University Hospital, France.
⁸ Department of Neurology and Laboratory of Functional Neurosciences, University Hospital of Amiens, France.
⁹ Department of Neurology, University Hospital of Amiens, France.
¹⁰ University of Lille, INSERM CIC-IT 807, France.
¹¹ University Hospital of Amiens, France.
¹² Department of Biostatistics and Medical Research, University Hospital of Amiens, France.
¹³ Department of Psychiatry and Laboratory of Functional Neurosciences, University Hospital of Amiens, France.
¹⁴ Department of Radiology, University Hospital of Amiens, France.
¹⁵ Department of Neurology, Val de Grace Hospital, Paris, France.
¹⁶ Department of Neurology, Hospital of La Rochelle, France.
¹⁷ Department of Neurology, University Hospital of St Etienne, France.
¹⁸ Department of Neurology and CMRR, University Hospital of St Etienne, France.
¹⁹ Department of Psychology and Laboratory CRPPCO, University of Amiens, France.
²⁰ Department of Psychology, University of Caen, France.
²¹ Department of Psychology, University of Lille, France.
²² Department of Neurology, Hospital of Creil, France.
²³ Department of Neurology, Hospital of Epinal, France.
²⁴ Department of Neurology, Hospital of Ajaccio, France.
²⁵ Institut de Logopédie, Haute Ecole de Liège, Belgium.

PMID: 37207410
DOI: 10.1016/j.cortex.2023.03.013

Abstract

The functional organization and related anatomy of executive functions are still largely unknown and were examined in the present study using a verbal fluency task. The objective of this study was to determine the cognitive architecture of a fluency task and related voxelwise anatomy in the GRECogVASC cohort and fMRI based meta-analytical data. First, we proposed a model of verbal fluency in which two control processes, lexico-semantic strategic search process and attention process, interact with semantic and lexico-phonological output processes. This model was assessed by testing 404 patients and 775 controls for semantic and letter fluency, naming, and processing speed (Trail Making test part A). Regression (R² = .276 and .3, P = .0001, both) and structural equation modeling (CFI: .88, RMSEA: .2, SRMR: .1) analyses supported this model. Second, voxelwise lesion-symptom mapping and disconnectome analyses demonstrated fluency to be associated with left lesions of the pars opercularis, lenticular nucleus, insula, temporopolar region, and a large number of tracts. In addition, a single dissociation showed specific association of letter fluency with the pars triangularis of F3. Disconnectome mapping showed the additional role of disconnection of left frontal gyri and thalamus. By contrast, these analyses did not identify voxels specifically associated with lexico-phonological search processes. Third, meta-analytic fMRI data (based on 72 studies) strikingly matched all structures identified by the lesion approach. These results support our modeling of the functional architecture of verbal fluency based on two control processes (strategic search and attention) operating on semantic and lexico-phonologic output processes. Multivariate analysis supports the prominent role of the temporopolar area (BA 38) in semantic fluency and the F3 triangularis area (BA 45) in letter fluency. Finally, the lack of voxels specifically dedicated to strategic search processes could be due to a distributed organization of executive functions warranting further studies.

Keywords: Control functions; Dementia; Executive functions; Fluency; Stroke.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain Mapping* / methods
Broca Area
Humans
Neuropsychological Tests
Prefrontal Cortex
Semantics
Stroke* / diagnostic imaging
Stroke* / psychology