Hand function after neonatal stroke: A graph model based on basal ganglia and thalami structure
Introduction: Neonatal arterial ischemic stroke (NAIS) is a common model to study the impact of a unilateral early brain insult on developmental brain plasticity and the appearance of long-term outcomes. Motor difficulties that may arise are typically related to poor function of the affected (contra...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S221315822400007X |
| _version_ | 1827319206898565120 |
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| author | Patty Coupeau Josselin Démas Jean-Baptiste Fasquel Lucie Hertz-Pannier Stéphane Chabrier Mickael Dinomais |
| author_facet | Patty Coupeau Josselin Démas Jean-Baptiste Fasquel Lucie Hertz-Pannier Stéphane Chabrier Mickael Dinomais |
| author_sort | Patty Coupeau |
| collection | DOAJ |
| description | Introduction: Neonatal arterial ischemic stroke (NAIS) is a common model to study the impact of a unilateral early brain insult on developmental brain plasticity and the appearance of long-term outcomes. Motor difficulties that may arise are typically related to poor function of the affected (contra-lesioned) hand, but surprisingly also of the ipsilesional hand. Although many longitudinal studies after NAIS have shown that predicting the occurrence of gross motor difficulties is easier, accurately predicting hand motor function (for both hands) from morphometric MRI remains complicated. The hypothesis of an association between the structural organization of the basal ganglia (BG) and thalamus with hand motor function seems intuitive given their key role in sensorimotor function. Neuroimaging studies have frequently investigated these structures to evaluate the correlation between their volumes and motor function following early brain injury. However, the results have been controversial. We hypothesize the involvement of other structural parameters. Method: The study involves 35 children (mean age 7.3 years, SD 0.4) with middle cerebral artery NAIS who underwent a structural T1-weighted 3D MRI and clinical examination to assess manual dexterity using the Box and Blocks Test (BBT). Graphs are used to represent high-level structural information of the BG and thalami (volumes, elongations, distances) measured from the MRI. A graph neural network (GNN) is proposed to predict children’s hand motor function through a graph regression. To reduce the impact of external factors on motor function (such as behavior and cognition), we calculate a BBT score ratio for each child and hand. Results: The results indicate a significant correlation between the score ratios predicted by our method and the actual score ratios of both hands (p < 0.05), together with a relatively high accuracy of prediction (mean L1 distance < 0.03). The structural information seems to have a different influence on each hand’s motor function. The affected hand’s motor function is more correlated with the volume, while the ‘unaffected’ hand function is more correlated with the elongation of the structures. Experiments emphasize the importance of considering the whole macrostructural organization of the basal ganglia and thalami networks, rather than the volume alone, to predict hand motor function. Conclusion: There is a significant correlation between the structural characteristics of the basal ganglia/thalami and motor function in both hands. These results support the use of MRI macrostructural features of the basal ganglia and thalamus as an early biomarker for predicting motor function in both hands after early brain injury. |
| first_indexed | 2024-03-08T11:25:49Z |
| format | Article |
| id | doaj.art-79c458a0ad28404fa821a7792ff389bc |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-04-25T00:15:48Z |
| publishDate | 2024-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-79c458a0ad28404fa821a7792ff389bc2024-03-13T04:45:37ZengElsevierNeuroImage: Clinical2213-15822024-01-0141103568Hand function after neonatal stroke: A graph model based on basal ganglia and thalami structurePatty Coupeau0Josselin Démas1Jean-Baptiste Fasquel2Lucie Hertz-Pannier3Stéphane Chabrier4Mickael Dinomais5Université d'Angers, LARIS, SFR MATHSTIC, F-49000 Angers, France; Corresponding author at: LARIS – Polytech Angers, 62 avenue de Notre Dame du Lac 49000 ANGERS, France.Université d'Angers, LARIS, SFR MATHSTIC, F-49000 Angers, France; Instituts de Formation, CH Laval, FranceUniversité d'Angers, LARIS, SFR MATHSTIC, F-49000 Angers, FranceUNIACT/Neurospin/JOLIOT/DRF/CEA-Saclay, and U1141 NeuroDiderot/Inserm, CEA, Paris University, FranceFrench Centre for Pediatric Stroke, Pediatric Physical and Rehabilitation Medicine Department, Saint-Etienne University Hospital, FranceUniversité d'Angers, LARIS, SFR MATHSTIC, F-49000 Angers, France; Department of Physical and Rehabilitation Medicine, University Hospital, CHU Angers, FranceIntroduction: Neonatal arterial ischemic stroke (NAIS) is a common model to study the impact of a unilateral early brain insult on developmental brain plasticity and the appearance of long-term outcomes. Motor difficulties that may arise are typically related to poor function of the affected (contra-lesioned) hand, but surprisingly also of the ipsilesional hand. Although many longitudinal studies after NAIS have shown that predicting the occurrence of gross motor difficulties is easier, accurately predicting hand motor function (for both hands) from morphometric MRI remains complicated. The hypothesis of an association between the structural organization of the basal ganglia (BG) and thalamus with hand motor function seems intuitive given their key role in sensorimotor function. Neuroimaging studies have frequently investigated these structures to evaluate the correlation between their volumes and motor function following early brain injury. However, the results have been controversial. We hypothesize the involvement of other structural parameters. Method: The study involves 35 children (mean age 7.3 years, SD 0.4) with middle cerebral artery NAIS who underwent a structural T1-weighted 3D MRI and clinical examination to assess manual dexterity using the Box and Blocks Test (BBT). Graphs are used to represent high-level structural information of the BG and thalami (volumes, elongations, distances) measured from the MRI. A graph neural network (GNN) is proposed to predict children’s hand motor function through a graph regression. To reduce the impact of external factors on motor function (such as behavior and cognition), we calculate a BBT score ratio for each child and hand. Results: The results indicate a significant correlation between the score ratios predicted by our method and the actual score ratios of both hands (p < 0.05), together with a relatively high accuracy of prediction (mean L1 distance < 0.03). The structural information seems to have a different influence on each hand’s motor function. The affected hand’s motor function is more correlated with the volume, while the ‘unaffected’ hand function is more correlated with the elongation of the structures. Experiments emphasize the importance of considering the whole macrostructural organization of the basal ganglia and thalami networks, rather than the volume alone, to predict hand motor function. Conclusion: There is a significant correlation between the structural characteristics of the basal ganglia/thalami and motor function in both hands. These results support the use of MRI macrostructural features of the basal ganglia and thalamus as an early biomarker for predicting motor function in both hands after early brain injury.http://www.sciencedirect.com/science/article/pii/S221315822400007XPerinatal strokeCerebral palsyMotor cortexBasal gangliaStructural organizationGraph neural network |
| spellingShingle | Patty Coupeau Josselin Démas Jean-Baptiste Fasquel Lucie Hertz-Pannier Stéphane Chabrier Mickael Dinomais Hand function after neonatal stroke: A graph model based on basal ganglia and thalami structure NeuroImage: Clinical Perinatal stroke Cerebral palsy Motor cortex Basal ganglia Structural organization Graph neural network |
| title | Hand function after neonatal stroke: A graph model based on basal ganglia and thalami structure |
| title_full | Hand function after neonatal stroke: A graph model based on basal ganglia and thalami structure |
| title_fullStr | Hand function after neonatal stroke: A graph model based on basal ganglia and thalami structure |
| title_full_unstemmed | Hand function after neonatal stroke: A graph model based on basal ganglia and thalami structure |
| title_short | Hand function after neonatal stroke: A graph model based on basal ganglia and thalami structure |
| title_sort | hand function after neonatal stroke a graph model based on basal ganglia and thalami structure |
| topic | Perinatal stroke Cerebral palsy Motor cortex Basal ganglia Structural organization Graph neural network |
| url | http://www.sciencedirect.com/science/article/pii/S221315822400007X |
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