Distinct neural systems for the production of communicative vocal behaviors

Abstract

Vocalizations are the production of sounds by the coordinated activity of up to eighty respiratory and laryngeal muscles. Whilst voiced acts, modified by the upper vocal tract (tongue, jaw, lip and palate) are central to the production of human speech, they are also central to the production of emotional vocalizations such as sounds of disgust, anger, laughter and crying. Evidence suggests that the speech and emotional vocalizations may comprise distinct classes of vocal movements: patients with speech production deficits are often able to produce emotional vocalizations. In addition to this, the ontogeny of the two articulations is largely distinct, with some culturally universal emotional vocalizations emerging soon after birth and human speech being a culture specific, highly learnt motor act, which must develop to some degree before a critical period in development. Here we investigate the motor pathways underlying these two classes of vocal movements for the first time by directly comparing BOLD responses during production of speech and non-speech vocal movements. Using functional magnetic resonance imaging, we report distinct patterns of activity in both subcortical and cortical regions (putamen and bilateral inferior frontal and parietal cortices) during the production of emotional vocalizations compared to speech production. In contrast we show that responses in primary sensorimotor regions do not differ during the production of speech and emotional vocalizations, suggesting partially overlapping, and partially non-overlapping neural structures for the motor control of these two classes of movement. In addition to this we report that responses in auditory cortices are distinct during the production of speech and non-speech vocalizations, suggesting that feedback control of speech and emotional vocalizations are distinct. These data provide novel evidence for the presence of dual pathways for the neural control of complex articulatory movements in humans. These findings are discussed in relation to the clinical and primate literature of vocal motor control.\n\nSignificance StatementThis work marks the first evidence in healthy humans for dual routes to vocal behaviors. Clinical evidence suggests that patients unable to produce speech may still be able to produce other vocal behaviors that employ the same set of effectors. Here we demonstrate that the production of different classes of vocal behavior is associated with overlapping and distinct networks of activity. Moreover, we show that auditory processing that occurs during the production of these movements may be distinct, suggesting that feedback may be used differently for these distinct classes of vocal movement.