No language-specific activation during linguistic processing of observed actions

Abstract

Background: It has been suggested that cortical neural systems for language evolved from motor cortical systems, in particular from those fronto-parietal systems responding also to action observation. While previous studies have shown shared cortical systems for action--or action observation--and language, they did not address the question of whether linguistic processing of visual stimuli occurs only within a subset of fronto-parietal areas responding to action observation. If this is true, the hypothesis that language evolved from fronto-parietal systems matching action execution and action observation would be strongly reinforced.

Methodology/ principal findings: We used functional magnetic resonance imaging (fMRI) while subjects watched video stimuli of hand-object-interactions and control photo stimuli of the objects and performed linguistic (conceptual and phonological), and perceptual tasks. Since stimuli were identical for linguistic and perceptual tasks, differential activations had to be related to task demands. The results revealed that the linguistic tasks activated left inferior frontal areas that were subsets of a large bilateral fronto-parietal network activated during action perception. Not a single cortical area demonstrated exclusive--or even simply higher--activation for the linguistic tasks compared to the action perception task.

Conclusions: These results show that linguistic tasks do not only share common neural representations but essentially activate a subset of the action observation network if identical stimuli are used. Our findings strongly support the evolutionary hypothesis that fronto-parietal systems matching action execution and observation were co-opted for language, a process known as exaptation.

Figure 1. Schematic overview on the experimental design.

Identical photo and video stimuli were employed across perceptual tasks (action observation/object perception), conceptual and phonological tasks. Thus differential functional imaging activations were not attributable to stimulus differences.

Figure 2. Behavioral data of correctness for all experimental tasks.

There were no differences regarding correctness across tasks. However, the tasks involving video stimuli (Vd-Perc, Vd-Conc, Vd-Phon) regarded longer reaction times than the photo stimulus tasks with the video action task evoking the longest reaction times. This reflects the nature of this task, focusing attention towards the performed hand action, whereas the other tasks directed attention towards the depicted object.

Figure 3

a) cortical networks activated by the decision task relating to action observation vs rest (Vd-Perc vs rest, red) and action observation vs perceptual decisions on photos of the same objects (Vd-Perc vs Ph-Perc, blue). The large bihemispheric networks found for both contrasts were very similar, suggesting that the fMRI activations found here mainly were related to action observation and not to processes of decision making or object perception required during these tasks, as well. b) Cortical networks activated during the phonological (blue) and the conceptual decision task (red) on photos of manipulable objects. The networks activated by these two linguistic tasks were entirely part of the action observation network depicted in Fig. 3a, in accordance with the hypothesis that development of language out of the mirror neuron system was driven by a process of exaptation.

Figure 4. Areas showing a significantly higher activation for decision on action observation (“is the hand holding the object with all five fingers?”) than for conceptual or phonological tasks involving the same video stimuli (Vd-Perc > (Vd-Phon+Vd-Conc)).

Comparison with the bilateral network for action observation (Fig. 3a) revealed that most the bilateral parietal and right frontal activations were activated when an action observation-related task was done but not if a concurrent cognitive task of conceptual or phonological decision on the same stimuli were performed.