Abstract
BackgroundIt 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 FindingsWe 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.ConclusionsThese 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.
Highlights
Since the initial observations on macaque mirror neurons - cells that fire while the monkey performs goal-directed actions and while the animal observes somebody else’s actions [1] - it has been speculated that these cells may have played a role in the evolution of language [2,3,4]
It is possible to test whether the overt linguistic processing of observed object-oriented action recruits cortical areas not engaged by action perception, and/or activates fronto-parietal action perception areas to a higher degree
Both results would support the hypothesis of some independence of linguistic processing of visual stimuli with respect to fronto-parietal areas concerned with action perception
Summary
Since the initial observations on macaque mirror neurons - cells that fire while the monkey performs goal-directed actions and while the animal observes somebody else’s actions [1] - it has been speculated that these cells may have played a role in the evolution of language [2,3,4]. 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. These results show that linguistic tasks do 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
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