The early adolescent brain on music: Analysis of functional dynamics reveals engagement of orbitofrontal cortex reward system

Abstract

Music listening plays a pivotal role for children and adolescents, yet surprisingly few neuroimaging studies have studied the underlying functional dynamics. We used functional magnetic resonance imaging to scan 17 preadolescents aged 10-11 years old while listening to music. We subsequently tracked the occurrence of functional brain networks over time by using a recent method that detects recurrent BOLD phase-locking states: the Leading Eigenvector Dynamics Analysis (LEiDA). In particular, we compared the probabilities of occurrence and switching profiles of different patterns of BOLD phase-locking between music and no music. Moreover, we used an adapted version of the Barcelona Music Reward Questionnaire (BMRQ) to measure the music reward sensitivity of the participants. Our results showed significantly increased occurrence of a BOLD phase-locking pattern during music listening compared to no music, characterized by a phase-shift in the BOLD signals of the medial orbitofrontal and ventromedial prefrontal cortices -a brain subsystem associated to reward processing -from the rest of the brain. Moreover, we observed a significantly higher probability of switching to this pattern while listening to music. We also found a positive correlation between the individual musical reward sensitivity and the tendency to switch to this reward state during music.Our findings highlight the involvement of a brain subsystem involved in hedonic processing during music listening in the early adolescent brain. These results offer novel insight into the neural underpinnings of musical reward in early adolescence and may help us to understand the importance of music at this delicate age.

Does Music Training Improve Inhibition Control in Children? A Systematic Review and Meta-Analysis

“…Music training is a rich and highly engaging experience for children and has the potential to strengthen cognitive skills that are essential for healthy child development. Merely listening to music in a brain imaging scanner elicits activation in the brain's reward circuits in both children (Fasano et al, 2022) and adults (Mas-Herrero et al, 2021;Vuust et al, 2022;Zatorre, 2015). Being internally motivated during learning experiences increases learning capacity and efficiency (Ryan & Deci, 2017), and this greater engagement is reflected in electrical brain activity following musical training (Kraus et al, 2014).…”

Age-related variability in network engagement during music listening

“…We ultimately chose the 4 state estimation as it provided a single state with activity in temporal and mesolimbic regions together. Temporal and mesolimbic region activity has been previously related to auditory reward (Salimpoor et al, 2011, Fasano et al, 2020), including prior analyses of subsets of the present data (Belden et al, 2023, Quinci et al, 2022).…”

“…Both younger and older adults showed the highest fractional occupancy in the temporal-mesolimbic network while listening to self-selected music compared to experimenter-selected music. These stimuli were selected by participants to be familiar and well-liked, and auditory-reward network activation for preferred music has been well-documented in prior studies (Salimpoor et al, 2011, Fasano et al, 2020), including on a subset of these data (Quinci et al, 2022). This network was active for experimenter-selected music as well, though to a lesser extent than self-selected music, particularly in younger adults.…”

Modulation of limbic resting-state networks by subthalamic nucleus deep brain stimulation

“…An advantage of the method is that it allows calculation of the proportion of time points during an fMRI session assigned to a given RSN, providing a quantitative measure that can be statistically compared between conditions (Alonso Martínez et al, 2020;Cabral, Vidaurre, et al, 2017;Figueroa et al, 2019;Larabi et al, 2020;Magalhães et al, 2021;Wong et al, 2021). This approach allows detection of network-specific modulations; for example, a previous study using LEiDA revealed that psilocybin, a psychoactive molecule, selectively decreases the occupancy of the frontoparietal RSN (associated with executive control), leaving the occupancy of the other RSNs unchanged (Lord et al, 2019), while another study revealed the specific engagement of the orbitofrontal cortex reward system during music listening (Fasano et al, 2022).…”