Utility of TMS to understand the neurobiology of speech

Despite intensive work on language-brain relations, and a fairly impressive accumulation of knowledge over the last several decades, there has been little progress in developing large-scale models of the functional anatomy of language that integrate neuropsychological, neuroimaging, and psycholinguistic data. Drawing on relatively recent developments in the cortical organization of vision, and on data from a variety of sources, we propose a new framework for understanding aspects of the functional anatomy of language which moves towards remedying this situation. The framework posits that early cortical stages of speech perception involve auditory fields in the superior temporal gyrus bilaterally (although asymmetrically). This cortical processing system then diverges into two broad processing streams, a ventral stream, which is involved in mapping sound onto meaning, and a dorsal stream, which is involved in mapping sound onto articulatory-based representations. The ventral stream projects ventro-laterally toward inferior posterior temporal cortex (posterior middle temporal gyrus) which serves as an interface between sound-based representations of speech in the superior temporal gyrus (again bilaterally) and widely distributed conceptual representations. The dorsal stream projects dorso-posteriorly involving a region in the posterior Sylvian fissure at the parietal-temporal boundary (area Spt), and ultimately projecting to frontal regions. This network provides a mechanism for the development and maintenance of "parity" between auditory and motor representations of speech. Although the proposed dorsal stream represents a very tight connection between processes involved in speech perception and speech production, it does not appear to be a critical component of the speech perception process under normal (ecologically natural) listening conditions, that is, when speech input is mapped onto a conceptual representation. We also propose some degree of bi-directionality in both the dorsal and ventral pathways. We discuss some recent empirical tests of this framework that utilize a range of methods. We also show how damage to different components of this framework can account for the major symptom clusters of the fluent aphasias, and discuss some recent evidence concerning how sentence-level processing might be integrated into the framework.

Action and perception are functionally linked in the brain, but a hotly debated question is whether perception and comprehension of stimuli depend on motor circuits. Brain language mechanisms are ideal for addressing this question. Neuroimaging investigations have found specific motor activations when subjects understand speech sounds, word meanings and sentence structures. Moreover, studies involving transcranial magnetic stimulation and patients with lesions affecting inferior frontal regions of the brain have shown contributions of motor circuits to the comprehension of phonemes, semantic categories and grammar. These data show that language comprehension benefits from frontocentral action systems, indicating that action and perception circuits are interdependent.

Direct recordings in monkeys have demonstrated that neurons in frontal and parietal areas discharge during execution and perception of actions [1-8]. Because these discharges "reflect" the perceptual aspects of actions of others onto the motor repertoire of the perceiver, these cells have been called mirror neurons. Their overlapping sensory-motor representations have been implicated in observational learning and imitation, two important forms of learning [9]. In humans, indirect measures of neural activity support the existence of sensory-motor mirroring mechanisms in homolog frontal and parietal areas [10, 11], other motor regions [12-15], and also the existence of multisensory mirroring mechanisms in nonmotor regions [16-19]. We recorded extracellular activity from 1177 cells in human medial frontal and temporal cortices while patients executed or observed hand grasping actions and facial emotional expressions. A significant proportion of neurons in supplementary motor area, and hippocampus and environs, responded to both observation and execution of these actions. A subset of these neurons demonstrated excitation during action-execution and inhibition during action-observation. These findings suggest that multiple systems in humans may be endowed with neural mechanisms of mirroring for both the integration and differentiation of perceptual and motor aspects of actions performed by self and others. Copyright © 2010 Elsevier Ltd. All rights reserved.