Cerebellar and basal ganglia structural connections in humans: Effect of aging and relation with memory and learning
IntroductionThe cerebellum and basal ganglia were initially considered anatomically distinct regions, each connected via thalamic relays which project to the same cerebral cortical targets, such as the motor cortex. In the last two decades, transneuronal viral transport studies in non-human primates...
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Aging Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnagi.2023.1019239/full |
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| author | Vineeth Radhakrishnan Cecile Gallea Romain Valabregue Syam Krishnan Chandrasekharan Kesavadas Bejoy Thomas Praveen James Ramshekhar Menon Asha Kishore Asha Kishore |
| author_facet | Vineeth Radhakrishnan Cecile Gallea Romain Valabregue Syam Krishnan Chandrasekharan Kesavadas Bejoy Thomas Praveen James Ramshekhar Menon Asha Kishore Asha Kishore |
| author_sort | Vineeth Radhakrishnan |
| collection | DOAJ |
| description | IntroductionThe cerebellum and basal ganglia were initially considered anatomically distinct regions, each connected via thalamic relays which project to the same cerebral cortical targets, such as the motor cortex. In the last two decades, transneuronal viral transport studies in non-human primates showed bidirectional connections between the cerebellum and basal ganglia at the subcortical level, without involving the cerebral cortical motor areas. These findings have significant implications for our understanding of neurodevelopmental and neurodegenerative diseases. While these subcortical connections were established in smaller studies on humans, their evolution with natural aging is less understood.MethodsIn this study, we validated and expanded the previous findings of the structural connectivity within the cerebellum-basal ganglia subcortical network, in a larger dataset of 64 subjects, across different age ranges. Tractography and fixel-based analysis were performed on the 3 T diffusion-weighted dataset using Mrtrix3 software, considering fiber density and cross-section as indicators of axonal integrity. Tractography of the well-established cerebello-thalamo-cortical tract was conducted as a control. We tested the relationship between the structural white matter integrity of these connections with aging and with the performance in different domains of Addenbrooke’s Cognitive Examination.ResultsTractography analysis isolated connections from the dentate nucleus to the contralateral putamen via the thalamus, and reciprocal tracts from the subthalamic nucleus to the contralateral cerebellar cortex via the pontine nuclei. Control tracts of cerebello-thalamo-cortical tracts were also isolated, including associative cerebello-prefrontal tracts. A negative linear relationship was found between the fiber density of both the ascending and descending cerebellum-basal ganglia tracts and age. Considering the cognitive assessments, the fiber density values of cerebello-thalamo-putaminal tracts correlated with the registration/learning domain scores. In addition, the fiber density values of cerebello-frontal and subthalamo-cerebellar (Crus II) tracts correlated with the cognitive assessment scores from the memory domain.ConclusionWe validated the structural connectivity within the cerebellum-basal ganglia reciprocal network, in a larger dataset of human subjects, across wider age range. The structural features of the subcortical cerebello-basal ganglia tracts in human subjects display age-related neurodegeneration. Individual morphological variability of cerebellar tracts to the striatum and prefrontal cortex was associated with different cognitive functions, suggesting a functional contribution of cerebellar tracts to cognitive decline with aging. This study offers new perspectives to consider the functional role of these pathways in motor learning and the pathophysiology of movement disorders involving the cerebellum and striatum. |
| first_indexed | 2024-04-10T20:16:53Z |
| format | Article |
| id | doaj.art-d00dacbbd2ce4e1490313c8e93f50f4b |
| institution | Directory Open Access Journal |
| issn | 1663-4365 |
| language | English |
| last_indexed | 2024-04-10T20:16:53Z |
| publishDate | 2023-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Aging Neuroscience |
| spelling | doaj.art-d00dacbbd2ce4e1490313c8e93f50f4b2023-01-26T04:48:54ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652023-01-011510.3389/fnagi.2023.10192391019239Cerebellar and basal ganglia structural connections in humans: Effect of aging and relation with memory and learningVineeth Radhakrishnan0Cecile Gallea1Romain Valabregue2Syam Krishnan3Chandrasekharan Kesavadas4Bejoy Thomas5Praveen James6Ramshekhar Menon7Asha Kishore8Asha Kishore9Comprehensive Care Centre for Movement Disorders, Department of Neurology, Sree Chitra Tirunal Institute of Medical Sciences and Technology, Thiruvananthapuram, IndiaINSERM, CNRS, Paris Brain Institute, Sorbonne Université, Paris, FranceINSERM, CNRS, Paris Brain Institute, Sorbonne Université, Paris, FranceComprehensive Care Centre for Movement Disorders, Department of Neurology, Sree Chitra Tirunal Institute of Medical Sciences and Technology, Thiruvananthapuram, IndiaDepartment of Imaging Sciences and Interventional Radiology, Sree Chitra Tirunal Institute of Medical Sciences and Technology, Thiruvananthapuram, IndiaDepartment of Imaging Sciences and Interventional Radiology, Sree Chitra Tirunal Institute of Medical Sciences and Technology, Thiruvananthapuram, IndiaComprehensive Care Centre for Movement Disorders, Department of Neurology, Sree Chitra Tirunal Institute of Medical Sciences and Technology, Thiruvananthapuram, IndiaDepartment of Neurology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, IndiaComprehensive Care Centre for Movement Disorders, Department of Neurology, Sree Chitra Tirunal Institute of Medical Sciences and Technology, Thiruvananthapuram, IndiaParkinson and Movement Disorder Centre, Department of Neurology, Aster Medcity, Kochi, IndiaIntroductionThe cerebellum and basal ganglia were initially considered anatomically distinct regions, each connected via thalamic relays which project to the same cerebral cortical targets, such as the motor cortex. In the last two decades, transneuronal viral transport studies in non-human primates showed bidirectional connections between the cerebellum and basal ganglia at the subcortical level, without involving the cerebral cortical motor areas. These findings have significant implications for our understanding of neurodevelopmental and neurodegenerative diseases. While these subcortical connections were established in smaller studies on humans, their evolution with natural aging is less understood.MethodsIn this study, we validated and expanded the previous findings of the structural connectivity within the cerebellum-basal ganglia subcortical network, in a larger dataset of 64 subjects, across different age ranges. Tractography and fixel-based analysis were performed on the 3 T diffusion-weighted dataset using Mrtrix3 software, considering fiber density and cross-section as indicators of axonal integrity. Tractography of the well-established cerebello-thalamo-cortical tract was conducted as a control. We tested the relationship between the structural white matter integrity of these connections with aging and with the performance in different domains of Addenbrooke’s Cognitive Examination.ResultsTractography analysis isolated connections from the dentate nucleus to the contralateral putamen via the thalamus, and reciprocal tracts from the subthalamic nucleus to the contralateral cerebellar cortex via the pontine nuclei. Control tracts of cerebello-thalamo-cortical tracts were also isolated, including associative cerebello-prefrontal tracts. A negative linear relationship was found between the fiber density of both the ascending and descending cerebellum-basal ganglia tracts and age. Considering the cognitive assessments, the fiber density values of cerebello-thalamo-putaminal tracts correlated with the registration/learning domain scores. In addition, the fiber density values of cerebello-frontal and subthalamo-cerebellar (Crus II) tracts correlated with the cognitive assessment scores from the memory domain.ConclusionWe validated the structural connectivity within the cerebellum-basal ganglia reciprocal network, in a larger dataset of human subjects, across wider age range. The structural features of the subcortical cerebello-basal ganglia tracts in human subjects display age-related neurodegeneration. Individual morphological variability of cerebellar tracts to the striatum and prefrontal cortex was associated with different cognitive functions, suggesting a functional contribution of cerebellar tracts to cognitive decline with aging. This study offers new perspectives to consider the functional role of these pathways in motor learning and the pathophysiology of movement disorders involving the cerebellum and striatum.https://www.frontiersin.org/articles/10.3389/fnagi.2023.1019239/fullagingmemorylearningcerebellumbasal gangliatractography |
| spellingShingle | Vineeth Radhakrishnan Cecile Gallea Romain Valabregue Syam Krishnan Chandrasekharan Kesavadas Bejoy Thomas Praveen James Ramshekhar Menon Asha Kishore Asha Kishore Cerebellar and basal ganglia structural connections in humans: Effect of aging and relation with memory and learning Frontiers in Aging Neuroscience aging memory learning cerebellum basal ganglia tractography |
| title | Cerebellar and basal ganglia structural connections in humans: Effect of aging and relation with memory and learning |
| title_full | Cerebellar and basal ganglia structural connections in humans: Effect of aging and relation with memory and learning |
| title_fullStr | Cerebellar and basal ganglia structural connections in humans: Effect of aging and relation with memory and learning |
| title_full_unstemmed | Cerebellar and basal ganglia structural connections in humans: Effect of aging and relation with memory and learning |
| title_short | Cerebellar and basal ganglia structural connections in humans: Effect of aging and relation with memory and learning |
| title_sort | cerebellar and basal ganglia structural connections in humans effect of aging and relation with memory and learning |
| topic | aging memory learning cerebellum basal ganglia tractography |
| url | https://www.frontiersin.org/articles/10.3389/fnagi.2023.1019239/full |
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