Less wiring, more firing: low-performing older adults compensate for impaired white matter with greater neural activity

Cereb Cortex. 2015 Apr;25(4):983-90. doi: 10.1093/cercor/bht289. Epub 2013 Oct 23.

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.

Keywords: DTI; MTL; PFC; elderly; fMRI; frontal.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Aged
  • Aging / pathology
  • Aging / physiology
  • Brain Mapping
  • Diffusion Tensor Imaging
  • Executive Function / physiology
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Memory / physiology
  • Neural Pathways / pathology
  • Neural Pathways / physiology
  • Neuropsychological Tests
  • Prefrontal Cortex / pathology*
  • Prefrontal Cortex / physiology*
  • Temporal Lobe / pathology*
  • Temporal Lobe / physiology*
  • White Matter / pathology*
  • White Matter / physiology*