Music-induced cognitive change and whole-brain network flexibility: a pilot study

Abstract

Introduction: Cognitive impairment that exceeds age-related cognitive decline is a risk factor for Alzheimer's disease and related dementias. As the older adult population is notably increasing every year, significant efforts are being made to preserve cognitive function in older adulthood. Non-pharmaceutical approaches such as music interventions have noticeable benefits for cognition. Music engagement utilizes multiple brain regions dually involved in higher cognitive functions. Yet the neurobiology of music-induced cognitive change remains understudied. Complex human behavior and cognition likely depend on continuous communication across brain regions rather than localized activity in one region. Given that music creativity engages a wide range of mental processes, whole-brain network indices quantifying the brain's tendency to create functional communities (modularity) and then dynamically reorganize these communities (flexibility) may be relevant for assessing music-related cognitive change. Using a semi-randomized clinical trial design (ClinicalTrials.gov; NCT04137913), we examined whether (1) music creativity altered whole-brain network indices (modularity, flexibility) and (2) whether music-related effects on cognition depended on whole-brain network indices.

Methods: Fifty-two older adults (Mean age = 75 years; 54% female; 84% White) were randomized to a 6-week music creativity intervention (n = 25) or a no-treatment control condition (n = 27) and completed resting-state fMRI scans and the Montreal Cognitive Assessment at baseline and follow-up (post-intervention).

Results: The music creativity intervention did not alter network flexibility or modularity over time. However, the relationship between group assignment and change in global cognitive function depended on baseline flexibility: music creativity improved global cognition more than the control condition, only among individuals who had higher than average network flexibility.

Discussion: Findings suggest that having a dynamic brain network, which has previously been linked to better executive functioning performance, may be necessary for music-related benefits on cognition. This pilot study is innovative as it is among the first to identify possible neural mechanisms underlying why music creativity interventions confer a more significant cognitive benefit for some older adults than others.

Keywords: cognition; creativity; fMRI; flexibility; mild cognitive impairment; music intervention; network analysis; older adulthood.

FIGURE 1

Flow chart of final analytic sample.

FIGURE 2

Calculation of whole-brain network flexibility and modularity from resting-state functional data. (A) The whole-brain is divided into 84 network nodes based on the parcellation of anatomical regions. Spontaneous activity from each brain region is captured during resting state functional neuroimaging over a run of 216 brain volumes. (B) For the modularity analysis, the entire time series is used to construct a whole-brain network. The correlation coefficient is used to determine network connections. In the example, Region 2 (orange) and Region 3 (green) have very similar signals throughout the entire imaging run, and so a link is drawn between them. Modularity and module membership are then determined. Modularity is defined as the percentage of network links that are between brain regions within the same module, and module membership is determined based on the groupings that would maximize modularity. In the cartoon example, there are 16 total links and 13 of which are intra-module links (color-coded according to their module), meaning 0.8 is the network modularity. The true calculation controls for the modularity value that would result from a random network. (C) For the flexibility analysis, a sliding window of 40 volumes is used to construct the changing whole-brain network over time. Modularity and module membership are determined for the brain network of each window. Flexibility is defined as the average rate that brain regions change their module memberships from one window to the next. In the cartoon example, brain region 1 (outlined in a purple halo) remains in the blue module for the first two time windows, but switches into the red module in the subsequent time window; among these three time windows, that brain region has a 0.5 flexibility rate.

FIGURE 3

The relationship between treatment group and global cognition (MMSE) at varying levels of baseline whole-brain network flexibility. Superscript symbols in the legend indicate statistical significance of simple slopes testing at +1/Mean/-1 SD values of the moderator (i.e., baseline flexibility). *p < 0.05. NS, not significant. “MMSE Total Score” reflects regress change results (i.e., MMSE scores at follow-up after controlling for baseline MMSE).