Musicianship and Prominence of Inter-Hemispheric Connectivity Determine Two Different Pathways to Atypical Language Dominance

During infancy and adolescence, language develops from a predominantly inter-hemispheric control — through the corpus callosum — to a predominantly intra-hemispheric control — mainly subserved by the left arcuate fasciculus. Using multimodal neuroimaging, we demonstrate that human left-handers (both male and female) with an atypical language lateralization show a rightward participation of language areas from auditory cortex to inferior frontal cortex when contrasting speech to tones perception, and an enhanced inter-hemispheric anatomical and functional connectivity. Crucially, musicianship determines two different structural pathways to this outcome. Non-musicians present a relation between atypical lateralization and intra-hemispheric underdevelopment across the anterior arcuate fasciculi, hinting at a dysregulation of the ontogenetic shift from an inter-hemispheric to an intra-hemispheric brain. Musicians reveal an alternative pathway related to inter-hemispheric overdevelopment across the posterior corpus callosum and the auditory cortex. We discuss the heterogeneity in reaching atypical language lateralization and the relevance of early musical training in altering the normal development of language cognitive functions.Significance statementSince the discovery in the 19thcentury that left-handedness predisposes to an atypical lateralization of language, progress in understanding how this condition appears in healthy individuals has been scarce. Here, we introduce a new relevant factor: musical training. We demonstrate how this early and intensive audiomotor learning can potentially modify the hemispheric specialization of language by prompting a differential development of the callosal fibers. Importantly, this perspective also reveals an alternative route to atypical lateralization — unrelated to musicianship — through an underdevelopment of the arcuate fasciculi. In both scenarios, interhemispheric connectivity through the callosum remains prominent, directly or indirectly. Therefore, the historical lack of definitive answers to this phenomenon might be attributed to the existence of multiple potential pathways.