Musical Expertise Increases Top–Down Modulation Over Hippocampal Activation during Familiarity Decisions

Pierre Gagnepain, Baptiste Fauvel, Béatrice Desgranges, Malo Gaubert, Fausto Viader, Francis Eustache, Mathilde Groussard, Hervé Platel

The hippocampus has classically been associated with episodic memory, but is sometimes also recruited during semantic memory tasks, especially for the skilled exploration of familiar information. Cognitive control mechanisms guiding semantic memory search may benefit from the set of cognitive processes at stake during musical training. Here, we examined using functional magnetic resonance imaging, whether musical expertise would promote the top-down control of the left inferior frontal gyrus (LIFG) over the generation of hippocampally based goal-directed thoughts mediating the familiarity judgment of proverbs and musical items. Analyses of behavioral data confirmed that musical experts more efficiently access familiar melodies than non-musicians although such increased ability did not transfer to verbal semantic memory. At the brain level, musical expertise specifically enhanced the recruitment of the hippocampus during semantic access to melodies, but not proverbs. Additionally, hippocampal activation contributed to speed of access to familiar melodies, but only in musicians. Critically, causal modeling of neural dynamics between LIFG and the hippocampus further showed that top-down excitatory regulation over the hippocampus during familiarity decision specifically increases with musical expertise - an effect that generalized across melodies and proverbs. At the local level, our data show that musical expertise modulates the online recruitment of hippocampal response to serve semantic memory retrieval of familiar melodies. The reconfiguration of memory network dynamics following musical training could constitute a promising framework to understand its ability to preserve brain functions.