Human motor cortex relies on sparse and action-specific activation during laughing, smiling and speech production

Markus Kern,Tonio Ball,Sina Bert,Olga Glanz,Andreas Schulze-Bonhage

doi:10.1038/s42003-019-0360-3

Abstract

Smiling, laughing, and overt speech production are fundamental to human everyday communication. However, little is known about how the human brain achieves the highly accurate and differentiated control of such orofacial movement during natural conditions. Here, we utilized the high spatiotemporal resolution of subdural recordings to elucidate how human motor cortex is functionally engaged during control of real-life orofacial motor behaviour. For each investigated movement class—lip licking, speech production, laughing and smiling—our findings reveal a characteristic brain activity pattern within the mouth motor cortex with both spatial segregation and overlap between classes. Our findings thus show that motor cortex relies on sparse and action-specific activation during real-life orofacial behaviour, apparently organized in distinct but overlapping subareas that control different types of natural orofacial movements.

Highlights

While an activated mouth motor cortex was repeatedly reported in the form of gamma activity in electrocorticography (ECoG) during experimental[5,6,7,8,9,10,11,12,13] as well as non-experimental[12,14] overt speech production, recent findings raise doubts if the mouth motor cortex is necessarily involved in controlling natural smiling and laughing
Is there a sub-regional specialization to major classes of natural motor behaviour like speech production vs. non-speech-related orofacial movements? And if so, on which spatial scale is such a potential action-based or task-specific organization principle implemented in human mouth motor cortex? Beyond electrical stimulation mapping to identify the mouth motor cortex, addressing these questions would require a functional mapping of brain activity with high spatial resolution during complex, real-life orofacial motor behaviours, which is methodologically challenging
Other studies have tried to reconstruct speech output from brain signals, opening new communication channels for locked-in patients[27]. Facial paralysis such as after stroke, head trauma, head tumour or infection/ inflammation of the facial nerve, affects a large number of individuals and can severely limit the freedom of facial expression and compromise the quality of social life of affected patients. It is currently not clear whether brain−computer interfaces (BCI) concepts developed for restoration of upper-extremity movement can be applied to natural orofacial motor behaviours, and how and to what degree smiling vs. laughing vs. other orofacial movements is decodable from cortical brain signals

Summary

Introduction

While an activated mouth motor cortex was repeatedly reported in the form of gamma activity in electrocorticography (ECoG) during experimental[5,6,7,8,9,10,11,12,13] as well as non-experimental[12,14] overt speech production, recent findings raise doubts if the mouth motor cortex is necessarily involved in controlling natural smiling and laughing. Recent studies took advantage of ECoG recordings directly obtained from the brain surface to study the neural basis of real-life movements of the upper[14,21] and lower extremities[14], as well as of eye movements[22] and nonexperimental speech production[12,14,23,24,25] It remains unclear how major classes of orofacial actions that play a crucial role in our daily life and social interaction, including laughing and smiling, are controlled by the human mouth motor cortex in reallife conditions. ECoG gamma band activity was previously found to be a useful marker of cortical brain activity during non-experimental, real-life conditions[14,25]; we focused our ECoG analyses on the event-related spectral modulations in the gamma frequency range[30,31,32,33,34] in addition to event-related potentials (ERPs)[35,36,37]

Methods

Results

Conclusion