Mental imagery of speech and movement implicates the dynamics of internal forward models

Xing Tian

doi:10.3389/fpsyg.2010.00166

Abstract

The classical concept of efference copies in the context of internal forward models has stimulated productive research in cognitive science and neuroscience. There are compelling reasons to argue for such a mechanism, but finding direct evidence in the human brain remains difficult. Here we investigate the dynamics of internal forward models from an unconventional angle: mental imagery, assessed while recording high temporal resolution neuronal activity using magnetoencephalography. We compare two overt and covert tasks; our covert, mental imagery tasks are unconfounded by overt input/output demands – but in turn necessitate the development of appropriate multi-dimensional topographic analyses. Finger tapping (studies 1 and 2) and speech experiments (studies 3–5) provide temporally constrained results that implicate the estimation of an efference copy. We suggest that one internal forward model over parietal cortex subserves the kinesthetic feeling in motor imagery. Secondly, observed auditory neural activity ~170 ms after motor estimation in speech experiments (studies 3–5) demonstrates the anticipated auditory consequences of planned motor commands in a second internal forward model in imagery of speech production. Our results provide neurophysiological evidence from the human brain in favor of internal forward models deploying efference copies in somatosensory and auditory cortex, in finger tapping and speech production tasks, respectively, and also suggest the dynamics and sequential updating structure of internal forward models.

Highlights

IntroductionForward models incorporate at their core the presupposition that neural systems internally simulate motor (output) commands and predict their perceptual consequences (for review see Wolpert and Ghahramani, 2000)
How do motor and sensory systems interact with cognitive systems to allow for an effective exchange of information between input and output operations? One of the influential theories proposed to address this challenge of mapping between potentially disparate “representational coordinate systems” builds on the concept of internal forward models
In the five connected MEG studies reported here, three findings emerge that support the dynamics in our proposed structure of internal forward models (Figure 1)

Summary

Introduction

Forward models incorporate at their core the presupposition that neural systems internally simulate motor (output) commands and predict their perceptual consequences (for review see Wolpert and Ghahramani, 2000). Guenther and colleagues have proposed an elegant architecture, the Directions Into Velocities of Articulators (DIVA) model, to account for speech production and motor learning in articulation (Guenther, 1995; Guenther et al, 1998, 2006) In their model, an efference copy of a motor command is used to constrain further motor preparation (Guenther et al, 1998) and an additional auditory efference copy is used to predict the possible auditory outcome (Guenther et al, 2006). The motor state is further updated following the signal calculated by taking account of three inputs (in green shaded area): the motor prediction from the first forward model, the somatosensory feedback, and the desired motor state which would compensate the discrepancy between the target auditory output, and actual auditory feedback

Methods

Results

Conclusion