From speech to thought: the neuronal basis of cognitive units in non-experimental, real-life communication investigated using ECoG

Johanna Derix^1,2,3*, Olga Iljina^1,4,5,6, Johanna Weiske^1,2,3, Andreas Schulze-Bonhage^1,3, Ad Aertsen^2,3 and Tonio Ball^1,3*

• ¹Department of Neurosurgery, Epilepsy Center, University Medical Center Freiburg, Freiburg, Germany
• ²Department of Neurobiology and Biophysics, Faculty of Biology, University of Freiburg, Freiburg, Germany
• ³Bernstein Center Freiburg, University of Freiburg, Freiburg, Germany
• ⁴GRK 1624, University of Freiburg, Freiburg, Germany
• ⁵Department of German Linguistics, University of Freiburg, Freiburg, Germany
• ⁶Hermann Paul School of Linguistics, University of Freiburg, Freiburg, Germany

Exchange of thoughts by means of expressive speech is fundamental to human communication. However, the neuronal basis of real-life communication in general, and of verbal exchange of ideas in particular, has rarely been studied until now. Here, our aim was to establish an approach for exploring the neuronal processes related to cognitive “idea” units (IUs) in conditions of non-experimental speech production. We investigated whether such units corresponding to single, coherent chunks of speech with syntactically-defined borders, are useful to unravel the neuronal mechanisms underlying real-world human cognition. To this aim, we employed simultaneous electrocorticography (ECoG) and video recordings obtained in pre-neurosurgical diagnostics of epilepsy patients. We transcribed non-experimental, daily hospital conversations, identified IUs in transcriptions of the patients' speech, classified the obtained IUs according to a previously-proposed taxonomy focusing on memory content, and investigated the underlying neuronal activity. In each of our three subjects, we were able to collect a large number of IUs which could be assigned to different functional IU subclasses with a high inter-rater agreement. Robust IU-onset-related changes in spectral magnitude could be observed in high gamma frequencies (70–150 Hz) on the inferior lateral convexity and in the superior temporal cortex regardless of the IU content. A comparison of the topography of these responses with mouth motor and speech areas identified by electrocortical stimulation showed that IUs might be of use for extraoperative mapping of eloquent cortex (average sensitivity: 44.4%, average specificity: 91.1%). High gamma responses specific to memory-related IU subclasses were observed in the inferior parietal and prefrontal regions. IU-based analysis of ECoG recordings during non-experimental communication thus elicits topographically- and functionally-specific effects. We conclude that segmentation of spontaneous real-world speech in linguistically-motivated units is a promising strategy for elucidating the neuronal basis of mental processing during non-experimental communication.