Abstract
Musical training and performance require precise integration of multisensory and motor centres of the human brain and can be regarded as an epigenetic modifier of brain functions. Numerous studies have identified structural and functional differences between the brains of musicians and non-musicians and superior cognitive functions in musicians. Recently, music-listening and performance has also been shown to affect the regulation of several genes, many of which were identified in songbird singing. MicroRNAs affect gene regulation and studying their expression may give new insights into the epigenetic effect of music. Here, we studied the effect of 2 hours of classical music-performance on the peripheral blood microRNA expressions in professional musicians with respect to a control activity without music for the same duration. As detecting transcriptomic changes in the functional human brain remains a challenge for geneticists, we used peripheral blood to study music-performance induced microRNA changes and interpreted the results in terms of potential effects on brain function, based on the current knowledge about the microRNA function in blood and brain. We identified significant (FDR <0.05) up-regulation of five microRNAs; hsa-miR-3909, hsa-miR-30d-5p, hsa-miR-92a-3p, hsa-miR-222-3p and hsa-miR-30a-5p; and down-regulation of two microRNAs; hsa-miR-6803-3p and hsa-miR-1249-3p. hsa-miR-222-3p and hsa-miR-92a-3p putatively target FOXP2, which was found down-regulated by microRNA regulation in songbird singing. miR-30d and miR-222 corroborate microRNA response observed in zebra finch song-listening/learning. miR-222 is induced by ERK cascade, which is important for memory formation, motor neuron functions and neuronal plasticity. miR-222 is also activated by FOSL1, an immediate early gene from the FOS family of transcriptional regulators which are activated by auditory-motor stimuli. miR-222 and miR-92 promote neurite outgrowth by negatively regulating the neuronal growth inhibitor, PTEN, and by activating CREB expression and phosphorylation. The up-regulation of microRNAs previously found to be regulators of auditory and nervous system functions (miR-30d, miR-92a and miR-222) is indicative of the sensory perception processes associated with music-performance. Akt signalling pathway which has roles in cell survival, cell differentiation, activation of CREB signalling and dopamine transmission was one of the functions regulated by the up-regulated microRNAs; in accordance with functions identified from songbird learning. The up-regulated microRNAs were also found to be regulators of apoptosis, suggesting repression of apoptotic mechanisms in connection with music-performance. Furthermore, comparative analyses of the target genes of differentially expressed microRNAs with that of the song-responsive microRNAs in songbirds suggest convergent regulatory mechanisms underlying auditory perception.
Highlights
IntroductionPlaying an instrument requires meticulous integration between the sensory (visual, auditory, tactile) and motor systems (timing, sequencing and spatial organisation of movements) (Zatorre, Chen & Penhune, 2007; Hyde et al, 2009)
Playing an instrument requires meticulous integration between the sensory and motor systems (Zatorre, Chen & Penhune, 2007; Hyde et al, 2009)
Music-performance The music-performance study was comprised of professional musicians (N 1⁄4 10) from Tapiola sinfonietta who performed a Western classical music concert to the public
Summary
Playing an instrument requires meticulous integration between the sensory (visual, auditory, tactile) and motor systems (timing, sequencing and spatial organisation of movements) (Zatorre, Chen & Penhune, 2007; Hyde et al, 2009). Long-term focused sensorimotor training often required for mastering a musical instrument causes structural and functional changes in the brain and cerebral cognitive networks (Schlaug, 2001; Gaser & Schlaug, 2003; Meyer, Elmer & Jäncke, 2012; Herholz & Zatorre, 2012; Moore et al, 2014). Research based on the effect of music training on the musician’s brain has often used neuroimaging techniques and descriptive analyses (Elbert et al, 1995; Schlaug, 2001; Gaser & Schlaug, 2003; Hyde et al, 2009; Meyer, Elmer & Jäncke, 2012; Herholz & Zatorre, 2012; Steele et al, 2013; Moore et al, 2014; Park et al, 2014). Songbirds offer important models for studying genomic mechanisms underlying sound perception and production (vocal communication) and social communication in humans (Whitney et al, 2014)
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