High-level language processing regions are not engaged in action observation or imitation

Abstract

A set of left frontal, temporal, and parietal brain regions respond robustly during language comprehension and production (e.g., Fedorenko E, Hsieh PJ, Nieto-Castañón A, Whitfield-Gabrieli S, Kanwisher N. J Neurophysiol 104: 1177–1194, 2010; Menenti L, Gierhan SM, Segaert K, Hagoort P. Psychol Sci 22: 1173–1182, 2011). These regions have been further shown to be selective for language relative to other cognitive processes, including arithmetic, aspects of executive function, and music perception (e.g., Fedorenko E, Behr MK, Kanwisher N. Proc Natl Acad Sci USA 108: 16428–16433, 2011; Monti MM, Osherson DN. Brain Res 1428: 33–42, 2012). However, one claim about overlap between language and nonlinguistic cognition remains prominent. In particular, some have argued that language processing shares computational demands with action observation and/or execution (e.g., Rizzolatti G, Arbib MA. Trends Neurosci 21: 188–194, 1998; Koechlin E, Jubault T. Neuron 50: 963–974, 2006; Tettamanti M, Weniger D. Cortex 42: 491–494, 2006). However, the evidence for these claims is indirect, based on observing activation for language and action tasks within the same broad anatomical areas (e.g., on the lateral surface of the left frontal lobe). To test whether language indeed shares machinery with action observation/execution, we examined the responses of language brain regions, defined functionally in each individual participant (Fedorenko E, Hsieh PJ, Nieto-Castañón A, Whitfield-Gabrieli S, Kanwisher N. J Neurophysiol 104: 1177–1194, 2010) to action observation ( experiments 1, 2, and 3a) and action imitation ( experiment 3b). With the exception of the language region in the angular gyrus, all language regions, including those in the inferior frontal gyrus (within “Broca’s area”), showed little or no response during action observation/imitation. These results add to the growing body of literature suggesting that high-level language regions are highly selective for language processing (see Fedorenko E, Varley R. Ann NY Acad Sci 1369: 132–153, 2016 for a review). NEW & NOTEWORTHY Many have argued for overlap in the machinery used to interpret language and others’ actions, either because action observation was a precursor to linguistic communication or because both require interpreting hierarchically-structured stimuli. However, existing evidence is indirect, relying on group analyses or reverse inference. We examined responses to action observation in language regions defined functionally in individual participants and found no response. Thus language comprehension and action observation recruit distinct circuits in the modern brain.