Healthy aging and cognitive impairment alter EEG functional connectivity in distinct frequency bands

Abstract

Functional connectivity (FC) indicates the interdependencies between brain signals recorded from spatially distinct locations in different frequency bands, which is modulated by cognitive tasks and is known to change with aging and cognitive disorders. Recently, the power of narrow-band gamma oscillations induced by visual gratings has been shown to reduce with both healthy aging and in subjects with mild cognitive impairment (MCI). However, the impact of aging/MCI on stimulus-induced gamma FC has not been well studied. We recorded electroencephalogram (EEG) from a large cohort (N=229) of elderly subjects (>49 years) while they viewed large cartesian gratings to induce gamma oscillations and studied changes in alpha and gamma FC with healthy aging (N=218) and MCI (N=11). Surprisingly, we found that aging and disease changed power and FC in different ways. With healthy aging, alpha power did not change but FC decreased significantly. MCI reduced gamma but not alpha FC significantly compared with age and gender matched controls, even when power was matched between the two groups. Overall, our results show distinct effects of aging and disease on EEG power and FC, suggesting different mechanisms and the potential to use EEG stimulus-induced FC along with power for early diagnosis of Alzheimer's Disease.

Stimulus-induced gamma sources weaken but not shrink with healthy aging in human EEG

“…In other words, an overall weakening of gamma sources may have much less effect on FC compared to shrinkage. As shown previously, gamma FC reduced with age even when sensor power was accounted for (Kumar and Ray, 2023), which is more consistent with shrinkage rather than weakening of gamma sources. On the other hand, the relationship between power and FC may depend on factors beyond just source distribution.…”

“…Apart from power measured using EEG sensors, various ensemble features like functional connectivity (FC) (Kumar and Ray, 2023) and related compensatory mechanisms (Pathak et al, 2022) may also change with healthy aging, albeit in a different way compared to power (Murty et al, 2020). For example, FC decreases with aging in alpha and stimulus-induced gamma oscillations, even though alpha power does not and even when variation in gamma power is accounted for using regression (Kumar and Ray, 2023). Similarly, FC at Individual Alpha Peak Frequency (IAPF) may stay invariant with aging due to a compensatory mechanism where enhanced inter-areal coupling cancels the effect of increased axonal delays (Pathak et al, 2022).…”

Slope of the power spectral density flattens at low frequencies (<150 Hz) with healthy aging but also steepens at higher frequency (>200 Hz) in human electroencephalogram

“…We compared the PSDs and slopes in AD/MCI subjects with their age and gender matched healthy controls. As in our previous studies (Murty et al, 2021; Kumar and Ray, 2023), we averaged the PSDs/slopes across all controls for a given case subject to match the number of cases and controls. Figure 5 shows the results for the eyes closed condition (N=13).…”

“…We also compared the slopes in subjects with AD/MCI (termed “cases”) with their healthy, age and gender matched controls. As in our previous studies (Murty et al, 2021; Kumar and Ray, 2023), for each case, we averaged the relevant metrics for all age (± 1 year) and gender matched controls to yield a single control data point for each case, yielding 16 (13) pairs for eyes open (eyes closed) analyses (Table 1).…”

Enhanced stimulus-induced and stimulus-free gamma in open-eye meditators

“…Both slow and fast gamma weaken with age ( 18 ) and are abnormal in patients suffering from brain disorders like Alzheimer’s Disease (AD) ( 19 ) and Schizophrenia ( 20 ). In addition, connectivity across brain regions reduces with onset of AD predominantly in slow gamma ( 21 ).…”