Inferior frontal oscillations reveal visuo-motor matching for actions and speech: evidence from human intracranial recordings

Abstract

The neural correspondence between the systems responsible for the execution and recognition of actions has been suggested both in humans and non-human primates. Apart from being a key region of this visuo-motor observation-execution matching (OEM) system, the human inferior frontal gyrus (IFG) is also important for speech production. The functional overlap of visuo-motor OEM and speech, together with the phylogenetic history of the IFG as a motor area, has led to the idea that speech function has evolved from pre-existing motor systems and to the hypothesis that an OEM system may exist also for speech. However, visuo-motor OEM and speech OEM have never been compared directly. We used electrocorticography to analyze oscillations recorded from intracranial electrodes in human fronto-parieto-temporal cortex during visuo-motor (executing or visually observing an action) and speech OEM tasks (verbally describing an action using the first or third person pronoun). The results show that neural activity related to visuo-motor OEM is widespread in the frontal, parietal, and temporal regions. Speech OEM also elicited widespread responses partly overlapping with visuo-motor OEM sites (bilaterally), including frontal, parietal, and temporal regions. Interestingly a more focal region, the inferior frontal gyrus (bilaterally), showed both visuo-motor OEM and speech OEM properties independent of orolingual speech-unrelated movements. Building on the methodological advantages in human invasive electrocorticography, the present findings provide highly precise spatial and temporal information to support the existence of a modalityindependent action representation system in the human brain that is shared between systems for performing, interpreting and describing actions.

Insights and Perspectives on Sensory-Motor Integration and Rehabilitation

“…In other words, in pathological conditions affecting the acquirement of the information required to correctly represent the body, we are able to switch strategy in order to use a different reference frame (e.g., visuospatial) and accommodate ecologically appropriate adaptations, e.g., visually guided movements (Rothwell et al, 1982). This interpretation is in line with the evidence suggesting that movement representations are largely multimodal (Halje et al, 2015) and that the interplay between these different representations can change in the case of missing (Curtze et al, 2010), disconnected (Fiori et al, 2014) or misrepresented limbs (Daprati et al, 2010).…”

Spinal cord injury affects the interplay between visual and sensorimotor representations of the body

“…In this vein, motor imagery (an active mental rehearsal of movements without physical execution 12 ) is an ideal cognitive task. Cerebral representations of actions are largely multimodal 13 and imagined and executed movements show proportional timing (longer movements require longer time to be imagined) 14 and kinematic configuration (anatomically awkward movements are more difficult to imagine) 15 . In addition, despite specific differences 16 , they engage partially overlapping brain networks 17 18 19 .…”

Visual Neuropsychology in Development: Anatomo-Functional Brain Mechanisms of Action/Perception Binding in Health and Disease

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