Action planning and predictive coding when speaking

Abstract

Across the animal kingdom, sensations resulting from an animal's own actions are processed differently from sensations resulting from external sources, with self-generated sensations being suppressed. A forward model has been proposed to explain this process across sensorimotor domains. During vocalization, reduced processing of one's own speech is believed to result from a comparison of speech sounds to corollary discharges of intended speech production generated from efference copies of commands to speak. Until now, anatomical and functional evidence validating this model in humans has been indirect. Using EEG with anatomical MRI to facilitate source localization, we demonstrate that inferior frontal gyrus activity during the 300ms before speaking was associated with suppressed processing of speech sounds in auditory cortex around 100ms after speech onset (N1). These findings indicate that an efference copy from speech areas in prefrontal cortex is transmitted to auditory cortex, where it is used to suppress processing of anticipated speech sounds. About 100ms after N1, a subsequent auditory cortical component (P2) was not suppressed during talking. The combined N1 and P2 effects suggest that although sensory processing is suppressed as reflected in N1, perceptual gaps are filled as reflected in the lack of P2 suppression, explaining the discrepancy between sensory suppression and preserved sensory experiences. These findings, coupled with the coherence between relevant brain regions before and during speech, provide new mechanistic understanding of the complex interactions between action planning and sensory processing that provide for differentiated tagging and monitoring of one's own speech, processes disrupted in neuropsychiatric disorders.

A temporal predictive code for voice motor control: Evidence from ERP and behavioral responses to pitch-shifted auditory feedback

“…The P2 component was distributed more posteriorly with stronger activity over the central electrodes and an inversion over the bilateral temporo-parietal areas. Based on the findings from previous studies (Butler and Trainor, 2012; Wang et al, 2014), we suggest that the N1 responses arise from primary and secondary cortical auditory areas, and their modulation in this study is a neurophysiological index of sensory feedback suppression in response to temporally-predictable pitch-shift stimuli during vocal production and motor control. Less details are known about the neural generators of the P2 component, but its longer latency suggests that this neural response component reflect higher-level sensory-motor and cognitive processes and may receive contribution from multiple sources within sensory, motor and frontal cortices.…”

“…In addition, these findings suggest that exposure to repeated presentations of predictable stimuli results in the increased contribution of feedforward mechanisms during vocal motor control. This reasoning supports the framework for predictions by the internal forward model: learned predictions result in more accurate efference copies and, consequently, a decreased mismatch in sensory feedback (Chen et al, 2012; Korzyukov et al, 2012; Scheerer and Jones, 2014; Wang et al, 2014; Wolpert and Flanagan, 2001). …”

“…This notion was further supported by a study showing that the suppression was maximum for normal voice auditory feedback and was reduced or almost completely eliminated when a pitch-shift stimulus created mismatch between the internal predictions and the auditory feedback during vocalization (Behroozmand and Larson, 2011; Heinks-Maldonado et al, 2006). Additionally, a study by Wang et al (Wang et al, 2014) showed that the activation of inferior frontal gyrus (IFG) at about 300 ms before speaking is associated with the suppression of N1 responses in auditory cortex at about 100 ms following speech onset. Thus, it was concluded that the transmission of predictive codes from motor-related areas such as IFG is responsible for the suppression of neural activity in the auditory cortex during speaking.…”

Sex differences in associations of arginine vasopressin and oxytocin with resting‐state functional brain connectivity

“…In men, higher AVP was associated with less connectedness and efficiency in left IFG (pars triangularis) and left STG, two important regions for verbal abilities (Costafreda et al 2006; Wagner et al 2014; Wang et al 2014). Consistent with this idea is that higher connectedeness and efficiency in left pars triangularis was associated with better verbal fluency in men.…”

Predicting the sensory consequences of one’s own action: First evidence for multisensory facilitation

“…For example, visual predictions have often been studied using joysticks controlling a cursor, or natural feedback of the hand using a camera, with either temporal or spatial deviations of the feedback (Farrer, Bouchereau, Jeannerod, & Franck, 2008;Hoover & Harris, 2012;Leube et al, 2003). Actively producing speech and listening to recorded speech stimuli have been used to assess auditory prediction errors (Ford, Gray, Faustman, Heinks, & Mathalon, 2005;Wang et al, 2014). Finally, tactile stimuli with various delays have been used to investigate predictive mechanisms in the tactile domain (e.g., Blakemore, Wolpert, & Frith, 1998).…”