Neurovascular coupling in normal aging: a combined optical, ERP and fMRI study

Abstract

Brain aging is characterized by changes in both hemodynamic and neuronal responses, which may be influenced by the cardiorespiratory fitness of the individual. To investigate the relationship between neuronal and hemodynamic changes, we studied the brain activity elicited by visual stimulation (checkerboard reversals at different frequencies) in younger adults and in older adults varying in physical fitness. Four functional brain measures were used to compare neuronal and hemodynamic responses obtained from BA17: two reflecting neuronal activity (the event-related optical signal, EROS, and the C1 response of the ERP), and two reflecting functional hemodynamic changes (functional magnetic resonance imaging, fMRI, and near-infrared spectroscopy, NIRS). The results indicated that both younger and older adults exhibited a quadratic relationship between neuronal and hemodynamic effects, with reduced increases of the hemodynamic response at high levels of neuronal activity. Although older adults showed reduced activation, similar neurovascular coupling functions were observed in the two age groups when fMRI and deoxy-hemoglobin measures were used. However, the coupling between oxy- and deoxy-hemoglobin changes decreased with age and increased with increasing fitness. These data indicate that departures from linearity in neurovascular coupling may be present when using hemodynamic measures to study neuronal function.

Keywords: Aging; Event-related brain potentials (ERPs); Event-related optical signal (EROS); Fitness; Functional magnetic resonance imaging (fMRI); Near-infrared spectroscopy (NIRS); Neurovascular coupling.

Copyright © 2013 Elsevier Inc. All rights reserved.

Figures

Figure 1

Positions of the sources and detectors used in the study. Large circles represent detectors and small circles sources. Red and blue colors represent the two recording montages. The graph shows a schematic back view of the recording helmet. The approximate position of the inion is marked by a green cross.

Figure 2

(A) Time courses of the ERP response at the Pz electrode averaged across subjects (separately for each age group) and stimulation frequency conditions. (B) Grand average time courses across stimulation conditions of the EROS response at the peak voxel across subjects (same location across age groups) in the BA17 ROI; (C) Grand average time courses of the EROS response for the BA17 ROI, averaged across subjects (separately for each age group), stimulation conditions, and ROI voxels. (D) Time course of the standardized EROS response for each subject (averaged across stimulation conditions) at each individual subject’s peak location within the BA17 ROI.

Figure 3

(A) Amplitude of the ERP (SD of the C1 amplitude across electrodes in microvolts) and (B) amplitude of the peak EROS in BA17 (ps) responses, averaged across subjects, as a function of stimulation frequency, separately for younger and older adults. The error bars represent standard errors of the mean computed across subjects.

Figure 4

A: Z-score maps of the EROS data at a latency of 96 ms after stimulation, averaged across all subjects and stimulation conditions. The surface projection of BA17 is outlined in green on each of the maps. Left: Average map across all subjects for source-detector distances between 20 and 50 mm. Middle: Average map across all subjects for source-detector distances between 0 and 17.5 mm (control condition). Right: Difference between the other two maps. B: Average Z-score maps of the EROS data for younger (left) and older (middle) adults.

Figure 5

A: Z-score maps of the [HbO2] values between 5 and 15 seconds after the onset of stimulation. The surface projection of BA17 is outlined in green on each of the maps. Left: Average map across all subjects for source-detector distances between 20 and 50 mm. Middle: Average map across all subjects for source-detector distances between 0 and 17.5 mm (control condition). Right: Difference between the other two maps. B: Average Z-score maps of the [HbO2] data for young (left) and older (middle) adults. C: Average time course across all voxels of BA17 for young and older subjects.

Figure 6

A: Z-score maps of the [HbR] values between 5 and 15 seconds after the onset of stimulation. The surface projection of BA17 is outlined in green on each of the maps. Left: Average map across all subjects for source-detector distances between 20 and 50 mm. Middle: Average map across all subjects for source-detector distances between 0 and 17.5 mm (control condition). Right: Difference between the other two maps. B: Average Z-score maps of the [HbR] data for young (left) and older (middle) adults. C: Average time course across all voxels of BA17 for young and older subjects.

Figure 7

Changes in hemodynamic parameters in BA17 during the stimulation period with respect to baseline, as a function of stimulation frequency and age group. The vertical bars indicate standard errors of the means computed across subjects.

Figure 8

Scatter plots depicting the relationships between the predicted and observed hemodynamic responses for each stimulation condition (averaged across subjects).

Figure 9

Average correlations between the observed hemodynamic response and that predicted on the basis of the integration of the fast EROS response over time for younger and older adults. The vertical bars indicate standard errors of the mean computed across subjects.