title: Less wiring, more firing: low-performing older adults compensate for impaired white matter with greater neural activity.
abstract: The reliable neuroimaging finding that older adults often show greater activity (over-recruitment) than younger adults is typically attributed to compensation. Yet, the neural mechanisms of over-recruitment in older adults (OAs) are largely unknown. Rodent electrophysiology studies have shown that as number of afferent fibers within a circuit decreases with age, the fibers that remain show higher synaptic field potentials (less wiring, more firing). Extrapolating to system-level measures in humans, we proposed and tested the hypothesis that greater activity in OAs compensates for impaired white-matter connectivity. Using a neuropsychological test battery, we measured individual differences in executive functions associated with the prefrontal cortex (PFC) and memory functions associated with the medial temporal lobes (MTLs). Using event-related functional magnetic resonance imaging, we compared activity for successful versus unsuccessful trials during a source memory task. Finally, we measured white-matter integrity using diffusion tensor imaging. The study yielded 3 main findings. First, low-executive OAs showed greater success-related activity in the PFC, whereas low-memory OAs showed greater success-related activity in the MTLs. Second, low-executive OAs displayed white-matter deficits in the PFC, whereas low-memory OAs displayed white-matter deficits in the MTLs. Finally, in both prefrontal and MTL regions, white-matter decline and success-related activations occurred in close proximity and were negatively correlated. This finding supports the less-wiring-more-firing hypothesis, which provides a testable account of compensatory over-recruitment in OAs.
authors.affiliation: Center for Cognitive Neuroscience, Duke University, Durham, NC 27708, USA Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 HR, Netherlands.
authors.forename: Sander M
authors.initials: SM
authors.lastname: Daselaar
authors.affiliation: Center for Cognitive Neuroscience, Duke University, Durham, NC 27708, USA.
authors.forename: Vijeth
authors.initials: V
authors.lastname: Iyengar
authors.affiliation: Centre for Speech, Language and the Brain, Department of Psychology, University of Cambridge, Cambridge, CB2 3EB, UK.
authors.forename: Simon W
authors.initials: SW
authors.lastname: Davis
authors.affiliation: Center for Cognitive Neuroscience, Duke University, Durham, NC 27708, USA.
authors.forename: Karl
authors.initials: K
authors.lastname: Eklund
authors.affiliation: Memory Disorders Research Center, VA Boston Healthcare System, Boston University School of Medicine, Boston, MA 02130, USA Neuroimaging Research for Veterans Center, VA Boston Healthcare System, Boston, MA 02130, USA.
authors.forename: Scott M
authors.initials: SM
authors.lastname: Hayes
authors.affiliation: Center for Cognitive Neuroscience, Duke University, Durham, NC 27708, USA.
authors.forename: Roberto E
authors.initials: RE
authors.lastname: Cabeza
mesh_terms: D000368:Aged; D000375:Aging / Q000473:pathology / Q000502:physiology; D001931:Brain Mapping; D056324:Diffusion Tensor Imaging; D056344:Executive Function / Q000502:physiology; D005260:Female; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D008568:Memory / Q000502:physiology; D009434:Neural Pathways / Q000473:pathology / Q000502:physiology; D009483:Neuropsychological Tests; D017397:Prefrontal Cortex / Q000473:pathology* / Q000502:physiology*; D013702:Temporal Lobe / Q000473:pathology* / Q000502:physiology*; D066127:White Matter / Q000473:pathology* / Q000502:physiology*
keywords: DTI; MTL; PFC; elderly; fMRI; frontal