Sensory–motor networks involved in speech production and motor control: An fMRI study

• Published in: NeuroImage (Orlando, Fla.) Vol. 109; pp. 418 - 428
• Main Authors: Behroozmand, Roozbeh, Shebek, Rachel, Hansen, Daniel R., Oya, Hiroyuki, Robin, Donald A., Howard, Matthew A., Greenlee, Jeremy D.W.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.04.2015; Elsevier Limited
• Subjects: Acoustic Stimulation; Adult; Auditory feedback; Auditory Perception - physiology; Behavior; Brain - physiology; Brain Mapping; Control systems; Control theory; Feedback; Feedback, Sensory; Female; fMRI; Humans; Magnetic Resonance Imaging; Male; Motor Activity; Motors; Nerve Net; Networks; Phonetics; Pitch Perception - physiology; Pitch perturbation; Playbacks; Sensorimotor Cortex - physiology; Sensory–motor integration; Speech; Speech - physiology; Speech motor control; Speech Perception - physiology; Studies; Vowels; fMRI; Auditory feedback; Sensory–motor integration; Pitch perturbation; Speech motor control
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2015.01.040

Speaking is one of the most complex motor behaviors developed to facilitate human communication. The underlying neural mechanisms of speech involve sensory–motor interactions that incorporate feedback information for online monitoring and control of produced speech sounds. In the present study, we adopted an auditory feedback pitch perturbation paradigm and combined it with functional magnetic resonance imaging (fMRI) recordings in order to identify brain areas involved in speech production and motor control. Subjects underwent fMRI scanning while they produced a steady vowel sound /a/ (speaking) or listened to the playback of their own vowel production (playback). During each condition, the auditory feedback from vowel production was either normal (no perturbation) or perturbed by an upward (+600 cents) pitch-shift stimulus randomly. Analysis of BOLD responses during speaking (with and without shift) vs. rest revealed activation of a complex network including bilateral superior temporal gyrus (STG), Heschl's gyrus, precentral gyrus, supplementary motor area (SMA), Rolandic operculum, postcentral gyrus and right inferior frontal gyrus (IFG). Performance correlation analysis showed that the subjects produced compensatory vocal responses that significantly correlated with BOLD response increases in bilateral STG and left precentral gyrus. However, during playback, the activation network was limited to cortical auditory areas including bilateral STG and Heschl's gyrus. Moreover, the contrast between speaking vs. playback highlighted a distinct functional network that included bilateral precentral gyrus, SMA, IFG, postcentral gyrus and insula. These findings suggest that speech motor control involves feedback error detection in sensory (e.g. auditory) cortices that subsequently activate motor-related areas for the adjustment of speech parameters during speaking. •Auditory feedback plays a key role in speech production and motor control.•Humans vocally compensate for pitch perturbations in their voice auditory feedback.•Vocal pitch motor control involves a complex sensory–motor network in the brain.•Functional networks of speech motor control are not affected in patients with epilepsy.