ORIGINAL RESEARCH ARTICLE published: 13 June 2014 doi: 10.3389/fnhum.2014.00383 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 * 1 Department of Neurosurgery, Epilepsy Center, University Medical Center Freiburg, Freiburg, Germany 2 Department of Neurobiology and Biophysics, Faculty of Biology, University of Freiburg, Freiburg, Germany 3 Bernstein Center Freiburg, University of Freiburg, Freiburg, Germany 4 GRK 1624, University of Freiburg, Freiburg, Germany 5 Department of German Linguistics, University of Freiburg, Freiburg, Germany 6 Hermann Paul School of Linguistics, University of Freiburg, Freiburg, Germany Edited by: Klaus Gramann, Berlin Institute of Technology, Germany Reviewed by: Ivana Konvalinka, Technical University of Denmark, Denmark Wallace Chafe, University of California, Santa Barbara, USA *Correspondence: Johanna Derix and Tonio Ball, Epilepsy Center, University Medical Center Freiburg, Engelbergerstr. 21, 79106 Freiburg, Germany e-mail: johanna.derix@ uniklinik-freiburg.de; tonio.ball@uniklinik-freiburg.de 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 (70–150Hz) 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. Keywords: natural behavior, parietal cortex, prefrontal cortex, electrocorticography, high gamma mapping, autobiographical memory, idea unit, speech production INTRODUCTION Spontaneous language can reflect mental states and thus consti- tutes a fundamental link between externally-observable behavior and internal cognitive processes (Chafe, 1994, 2000, 2012). In the present study, we explored the utility of spoken language to investigate the neuronal correlates of higher-order cognitive functions. To this purpose, we analyzed real-world conversations from simultaneously-obtained video and intracranial electroen- cephalographic data. Intracranial electroencephalography recorded for diagnostic purposes from the human brain includes both electrocorticog- raphy (ECoG) and stereo-electroencephalography and is now increasingly being used to study higher-order cognition. Such functions have been addressed as speech perception (Crone et al., 2001a; Canolty et al., 2007; Pasley et al., 2012) and produc- tion (Crone et al., 2001b; Towle et al., 2008; Bouchard et al., 2013), social interaction (Cristofori et al., 2012; Derix et al., 2012; Mesgarani and Chang, 2012; Caruana et al., 2013), and episodic (Burke et al., 2013) and autobiographical (Steinvorth et al., 2010) memory. Non-experimental ECoG approaches to study speech (Towle et al., 2008; Bauer et al., 2013; Ruescher et al., 2013) and social cognition (Derix et al., 2012) have lately been proposed, which allow studying brain activity of humans behav- ing in out-of-the-lab conditions. Recently, we presented a new Frontiers in Human Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 383 | 1 HUMAN NEUROSCIENCE