Behavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativity
Abstract Background Although creativity is an essential cognitive function to adapt to an ever-changing world, its neurocognitive and cerebral bases still need clarification. Current models highlight the interaction between associative and executive processes underpinned by the default mode (DMN), e...
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BMC
2025-08-01
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| Series: | Behavioral and Brain Functions |
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| Online Access: | https://doi.org/10.1186/s12993-025-00292-z |
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| author | Victor Altmayer Marcela Ovando-Tellez Théophile Bieth Bénédicte Batrancourt Armelle Rametti-Lacroux Lucy Bernardaud Sarah Moreno-Rodriguez Lucie Vigreux Vincent Ledu Béatrice Garcin Raffaella Migliaccio Isabelle Le Ber Alizée Lopez-Persem Richard Levy Emmanuelle Volle ECOCAPTURE study group |
| author_facet | Victor Altmayer Marcela Ovando-Tellez Théophile Bieth Bénédicte Batrancourt Armelle Rametti-Lacroux Lucy Bernardaud Sarah Moreno-Rodriguez Lucie Vigreux Vincent Ledu Béatrice Garcin Raffaella Migliaccio Isabelle Le Ber Alizée Lopez-Persem Richard Levy Emmanuelle Volle ECOCAPTURE study group |
| author_sort | Victor Altmayer |
| collection | DOAJ |
| description | Abstract Background Although creativity is an essential cognitive function to adapt to an ever-changing world, its neurocognitive and cerebral bases still need clarification. Current models highlight the interaction between associative and executive processes underpinned by the default mode (DMN), executive control (ECN) and salience networks (SN). Furthermore, recent neuroimaging studies highlight the key role of the prefrontal cortex (PFC), located at the crossroads of these networks. Hence, behavioral variant frontotemporal dementia (bvFTD), characterized by progressive neurodegeneration principally impacting the prefrontal cortex and the intrinsic connectivity of these three creativity-related networks, represents a unique model to study creativity. In this study involving 14 bvFTD patients and 20 matched controls, we used a simple word-to-word association task (FGAT) to explore the specific cognitive processes involved in remote thinking, i.e., the production of creative semantic associations. Using voxel-based morphometry, we uncovered critical brain regions for each component and then characterized these regions’ intrinsic connectivity profiles using resting-state functional connectivity in healthy controls. Results We dissociated four key cognitive components underlying remote thinking: spontaneous associative thinking, inhibition of unoriginal responses, intentional remote associative thinking, and verbal initiation; and replicated them in three independent datasets. Spontaneous associative thinking relied on temporal and cerebellar regions involved in low-order and automatic semantic processing, connected with the DMN, ECN and SN. Inhibition of prepotent unoriginal responses depended on key nodes of the SN. The ability to intentionally generate remote semantic associations was underpinned by key regions of the DMN. Finally, initiation of verbal responses relied on the right dorsolateral PFC, connected to the ECN. BvFTD patients were impaired in the last three components. Two components, cognitive inhibition and intentional remote thinking, mediated the link between atrophy in critical regions and an independent measure of creative abilities. Conclusions These findings advance our understanding of creative neurocognition, distinguishing components of creative thinking and clarifying their critical cerebral bases, and participate in the characterization of creativity impairment in patients with bvFTD. |
| format | Article |
| id | doaj-art-fca29183eed043e490e62b1d5661ecb2 |
| institution | Kabale University |
| issn | 1744-9081 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | BMC |
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| series | Behavioral and Brain Functions |
| spelling | doaj-art-fca29183eed043e490e62b1d5661ecb22025-08-24T11:41:17ZengBMCBehavioral and Brain Functions1744-90812025-08-0121112310.1186/s12993-025-00292-zBehavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativityVictor Altmayer0Marcela Ovando-Tellez1Théophile Bieth2Bénédicte Batrancourt3Armelle Rametti-Lacroux4Lucy Bernardaud5Sarah Moreno-Rodriguez6Lucie Vigreux7Vincent Ledu8Béatrice Garcin9Raffaella Migliaccio10Isabelle Le Ber11Alizée Lopez-Persem12Richard Levy13Emmanuelle Volle14ECOCAPTURE study groupSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreSorbonne University, Institut du Cerveau – Paris Brain Institute – ICM, FrontLab, Inserm, CNRS, AP-HP, Hôpital de la Pitié SalpêtrièreAbstract Background Although creativity is an essential cognitive function to adapt to an ever-changing world, its neurocognitive and cerebral bases still need clarification. Current models highlight the interaction between associative and executive processes underpinned by the default mode (DMN), executive control (ECN) and salience networks (SN). Furthermore, recent neuroimaging studies highlight the key role of the prefrontal cortex (PFC), located at the crossroads of these networks. Hence, behavioral variant frontotemporal dementia (bvFTD), characterized by progressive neurodegeneration principally impacting the prefrontal cortex and the intrinsic connectivity of these three creativity-related networks, represents a unique model to study creativity. In this study involving 14 bvFTD patients and 20 matched controls, we used a simple word-to-word association task (FGAT) to explore the specific cognitive processes involved in remote thinking, i.e., the production of creative semantic associations. Using voxel-based morphometry, we uncovered critical brain regions for each component and then characterized these regions’ intrinsic connectivity profiles using resting-state functional connectivity in healthy controls. Results We dissociated four key cognitive components underlying remote thinking: spontaneous associative thinking, inhibition of unoriginal responses, intentional remote associative thinking, and verbal initiation; and replicated them in three independent datasets. Spontaneous associative thinking relied on temporal and cerebellar regions involved in low-order and automatic semantic processing, connected with the DMN, ECN and SN. Inhibition of prepotent unoriginal responses depended on key nodes of the SN. The ability to intentionally generate remote semantic associations was underpinned by key regions of the DMN. Finally, initiation of verbal responses relied on the right dorsolateral PFC, connected to the ECN. BvFTD patients were impaired in the last three components. Two components, cognitive inhibition and intentional remote thinking, mediated the link between atrophy in critical regions and an independent measure of creative abilities. Conclusions These findings advance our understanding of creative neurocognition, distinguishing components of creative thinking and clarifying their critical cerebral bases, and participate in the characterization of creativity impairment in patients with bvFTD.https://doi.org/10.1186/s12993-025-00292-zCreativityRemote thinkingSemantic associationsExecutive functionsFrontotemporal dementiaVoxel-based morphometry |
| spellingShingle | Victor Altmayer Marcela Ovando-Tellez Théophile Bieth Bénédicte Batrancourt Armelle Rametti-Lacroux Lucy Bernardaud Sarah Moreno-Rodriguez Lucie Vigreux Vincent Ledu Béatrice Garcin Raffaella Migliaccio Isabelle Le Ber Alizée Lopez-Persem Richard Levy Emmanuelle Volle ECOCAPTURE study group Behavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativity Behavioral and Brain Functions Creativity Remote thinking Semantic associations Executive functions Frontotemporal dementia Voxel-based morphometry |
| title | Behavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativity |
| title_full | Behavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativity |
| title_fullStr | Behavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativity |
| title_full_unstemmed | Behavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativity |
| title_short | Behavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativity |
| title_sort | behavioral variant frontotemporal dementia as a model for understanding the cognitive and cerebral determinants of verbal creativity |
| topic | Creativity Remote thinking Semantic associations Executive functions Frontotemporal dementia Voxel-based morphometry |
| url | https://doi.org/10.1186/s12993-025-00292-z |
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