M. Florencia Assaneo, Pablo Ripolles, Joan Orpella, Wy Ming Lin, Ruth de Diego Balaguer, David Poeppel

The ability to synchronize a motor output to an auditory input is a basic trait present in humans from birth with important cognitive implications. Infants’ proficiency in following a beat, for example, is a predictor of language skills. From a phylogenetic perspective, spontaneous synchronization (i.e. without explicit training) to an external rhythm is argued to be a unique characteristic of vocal learning species, including humans. The study of this distinctive attribute has typically focused on how body movements are entrained by non-speech signals - e.g. music or a beat. Here, instead, we investigate how humans spontaneously align their speech motor output to auditory speech input.

To begin with, we introduce a simple behavioral task, where individuals simultaneously perceive and produce syllables, with a remarkable outcome. The general population shows two qualitatively different behaviors: while some individuals are compelled to temporally align their utterances to the external stimulus, others show no interaction between the perceived and produced rhythms.

Subsequently, we investigate the neurophysiology and brain structure features underlying the segregation. First, with a magnetoencephalography protocol we show that, when passively listening to speech, synchronizers show increased brain-to-stimulus alignment over frontal areas as well as reduced rightward asymmetry in auditory cortex. Secondly, using diffusion weighted MRI technique, we find a distinct lateralization pattern in a white matter cluster -likely part of the arcuate fasciculus, pathway connecting frontal and auditory areas- that differentiated the groups, with synchronizers showing significantly greater left lateralization. Crucially, this structural difference relates to both the auditory and frontal neurophysiological results: increased leftward lateralization in the white matter was related to higher brain-to-stimulus synchrony in left frontal regions and to more symmetrical auditory entrainment. Finally, we demonstrate that the behavioral findings on audio-motor synchronization and its neural substrate have ecologically relevant consequences: the synchronizers perform better on a word-learning task.

In summary, the combined behavioral, neurophysiological, and neuroanatomic results reveal a fundamental phenomenon: whereas some individuals are compelled to spontaneously align their speech output to the speech input, others remained impervious to the external rhythm. Moreover, we show a deceptively simple behavioral task, capitalizing on individual differences, that turns out to be diagnostic of audio-motor synchronization, neurophysiological function, brain anatomy, and performance on a word-learning task. The use of such a test can help to better characterize individual performance, leading to new discoveries related to speech processing and language learning that could have been masked by pooling together populations with substantially different neural and behavioral attributes.