Prefronto-Striatal Structural Connectivity Mediates Adult Age Differences in Action Selection

• Published in: The Journal of neuroscience Vol. 41; no. 2; pp. 331 - 341
• Main Authors: Rasooli, Amirhossein, Zivari Adab, Hamed, Chalavi, Sima, Monteiro, Thiago S, Dhollander, Thijs, Mantini, Dante, Swinnen, Stephan P
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 13.01.2021
• Subjects: Adult; Adults; Age; Age differences; Aged; Aging; Aging - physiology; Caudate Nucleus - physiology; Cross-Sectional Studies; Cues; Decision Making; Diffusion Magnetic Resonance Imaging; Female; Frontal gyrus; Humans; Life span; Magnetic resonance imaging; Male; Middle Aged; Movement - physiology; Neostriatum; Neostriatum - anatomy & histology; Neostriatum - growth & development; Neostriatum - physiology; Neural Pathways - anatomy & histology; Neural Pathways - growth & development; Neural Pathways - physiology; Nucleus accumbens; Nucleus Accumbens - physiology; Older people; Photic Stimulation; Prefrontal Cortex - anatomy & histology; Prefrontal Cortex - growth & development; Prefrontal Cortex - physiology; Reaction time; Reaction Time - physiology; Reaction time task; Substantia alba; Young Adult; anatomical constrained tractography; prefronto-striatal connectivity; action selection; diffusion imaging; multilimb reaction time
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.1709-20.2020

In complex everyday environments, action selection is critical for optimal goal-directed behavior. This refers to the process of choosing a proper action from the range of possible alternatives. The neural mechanisms underlying action selection and how these are affected by normal aging remain to be elucidated. In the present cross-sectional study, we studied processes of effector selection during a multilimb reaction time task in a lifespan sample of healthy human adults ( = 89; 20-75 years; 48 males, 41 females). Participants were instructed to react as quickly and accurately as possible to visually cued stimuli representing single-limb or combined upper and/or lower limb motions. Diffusion MRI was used to study structural connectivity between prefrontal and striatal regions as critical nodes for action selection. Behavioral findings revealed that increasing age was associated with slowing of action selection performance. At the neural level, aging had a negative impact on prefronto-striatal connectivity. Importantly, mediation analyses revealed that the negative association between action selection performance and age was mediated by prefronto-striatal connectivity, specifically the connections between left rostral medial frontal gyrus and left nucleus accumbens as well as right frontal pole and left caudate. These results highlight the potential role of prefronto-striatal white matter decline in poorer action selection performance of older adults. As a result of enhanced life expectancy, researchers have devoted increasing attention to the study of age-related alterations in cognitive and motor functions. Here we study associations between brain structure and behavior to reveal the impact of central neural white matter changes as a function of normal aging on action selection performance. We demonstrate the critical role of a reduction in prefronto-striatal structural connectivity in accounting for action selection performance deficits in healthy older adults. Preserving this cortico-subcortical pathway may be critical for behavioral flexibility and functional independence in older age.