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.

Keywords: action imitation; action observation; fMRI; functional specificity; language network.

Fig. 1.

Sample stimuli for each experiment and condition. Experiment 1: A: example objects, grouped vertically by family; B: example family of dissimilar actions. Experiment 2: C: example body action stimuli; D: example face action stimuli. Experiment 3a/b: E: example face actions; F: example eye actions; G: example mouth actions; H: example hand actions.

Fig. 2.

Response to the language localizer conditions [estimated in data not used for functional region of interest (fROI) definition, as described in materials and methods] and action conditions across experiments. Next to each bar graph, we show the language parcel used to constrain the selection of individual language fROIs; the individual fROIs constitute 10% of each parcel (see materials and methods for details). Error bars indicate SE of the mean over participants. LIFG and LIFGorb, regions in left inferior frontal gyrus; LMFG, region in the left middle frontal gyrus; LAntTemp and LPostTemp, regions in the left temporal lobe; LAngG, region extending into the angular gyrus.

Fig. 3.

Responses in multiple-demand (MD) regions to the action conditions in experiments 2 and 3a/b. Next to each bar graph, we show the MD parcels used to constrain the selection of individual MD functional regions of interest (fROIs); the individual fROIs constitute 10% of each parcel (see materials and methods for details). Error bars indicate SE of the mean over participants. LIFGop, RIFGop, LPrecG, and RprecG, regions in the left and right inferior frontal gyrus and precentral gyrus; LSupPar and RSupPar, regions in the superior parietal cortex.

Fig. 4.

A: responses in speech-responsive functional regions of interest (fROIs) in the auditory cortex (defined by nonword perception > hand action observation contrast in experiment 3a, see materials and methods for details) to the nonword condition and the four action observation conditions in experiment 3a. Responses are estimated using data not used for fROI definition (see materials and methods). Error bars indicate SE of the mean over participants. L/R PP, left/right planum polare; L/R PT, left/right planum temporale; L/R ASTG, left/right anterior superior temporal gyrus; L/R PSTG, left/right posterior superior temporal gyrus. B: responses in articulation-responsive fROIs in the premotor cortex (defined by the nonword imitation > hand action imitation contrast in experiment 3b, see materials and methods for details) to the nonword imitation condition and the four action imitation conditions in experiment 3b. Responses are estimated using data not used for fROI definition (see materials and methods). Error bars indicate SE of the mean over participants. LPrCG, left precentral gyrus; RiPrCG, right inferior precentral gyrus; RsPrCG, right superior precentral gyrus.