Abstract
Age-related performance declines in visual tasks have been attributed to reductions in processing efficiency. The neural basis of these declines has been explored by comparing the blood-oxygen-level-dependent (BOLD) index of neural activity in older and younger adults during visual task performance. However, neural activity is one of many factors that change with age and lead to BOLD signal differences. We investigated the origin of age-related BOLD changes by comparing blood flow and oxygen metabolic constituents of BOLD signal. Subjects periodically viewed flickering annuli and pressed a button when detecting luminance changes in a central fixation cross. Using magnetic resonance dual-echo arterial spin labeling and CO2 ingestion, we observed age-equivalent (i.e., similar in older and younger groups) fractional cerebral blood flow (ΔCBF) in the presence of age-related increases in fractional cerebral metabolic rate of oxygen (ΔCMRO2). Reductions in ΔCBF responsiveness to increased ΔCMRO2 in elderly led to paradoxical age-related BOLD decreases. Age-related ΔCBF/ΔCMRO2 ratio decreases were associated with reaction times, suggesting that age-related slowing resulted from less efficient neural activity. We hypothesized that reduced vascular responsiveness to neural metabolic demand would lead to a reduction in ΔCBF/ΔCMRO2. A simulation of BOLD relative to ΔCMRO2 for lower and higher neurometabolic-flow coupling ratios (approximating those for old and young, respectively) indicated less BOLD signal change in old than young in relatively lower CMRO2 ranges, as well as greater BOLD signal change in young compared to old in relatively higher CMRO2 ranges. These results suggest that age-comparative studies relying on BOLD signal might be misinterpreted, as age-related BOLD changes do not merely reflect neural activity changes. Age-related declines in neurometabolic-flow coupling might lead to neural efficiency reductions that can adversely affect visual task performance.
Highlights
The human visual system exhibits age-related changes that lead to changes in the efficiency of information processing
We hypothesized that the relationship between activationinduced ∆cerebral blood flow (CBF) and ∆CMRO2 in primary visual cortex is fundamentally altered by the process of aging such that the BOLD response might differentially index neural activity in older compared to younger individuals
In order to present a clearer picture of the mean group values, this participant’s ∆CBF/∆CMRO2 ratio data are not included in the analyses presented in the Section “Results,” the inclusion of this participant’s data did not alter the significance of the results.) Similar ratios were calculated for BOLD and CBF data
Summary
The human visual system exhibits age-related changes that lead to changes in the efficiency of information processing. We hypothesized that the relationship between activationinduced ∆CBF and ∆CMRO2 in primary visual cortex is fundamentally altered by the process of aging such that the BOLD response might differentially index neural activity in older compared to younger individuals. In one study (Hutchison et al, 2012), we sought to observe age-related neurometabolic-flow coupling changes in visual cortex using calibrated fMRI and hypercapnia (cf Hoge et al, 1999a,b; Pasley et al, 2007; Ances et al, 2009). The relatively impoverished responsivity of ∆CBF for older adults still led to an age-related decrease in BOLD We speculated that such reduced vascular responsiveness to neural metabolic demand would lead to variation in ∆CBF/∆CMRO2 with variation in task demand. This simulation illustrates the potential impact of age-related changes in neurometabolic-flow coupling on the responsiveness of the BOLD signal
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