When does action comprehension need motor involvement? Evidence from upper limb aplasia

Abstract

Motor theories of action comprehension claim that comprehending the meaning of an action performed by a conspecific relies on the perceiver's own motor representation of the same action. According to this view, whether an action belongs to the motor repertoire of the perceiver should impact the ease by which this action is comprehended. We tested this prediction by assessing the ability of an individual (D.C.) born without upper limbs to comprehend actions involving hands (e.g., throwing) or other body parts (e.g., jumping). The tests used a range of different visual stimuli differing in the kind of information provided. The results showed that D.C. was as accurate and fast as control participants in comprehending natural video and photographic presentations of both manual and nonmanual actions, as well as pantomimes. However, he was selectively impaired at identifying point-light animations of manual actions. This impairment was not due to a difficulty in processing kinematic information per se. D.C. was indeed as accurate as control participants in two additional tests requiring a fine-grained analysis of an actor's arm or whole-body movements. These results challenge motor theories of action comprehension by showing that the visual analysis of body shape and motion provides sufficient input for comprehending observed actions. However, when body shape information is sparsely available, motor involvement becomes critical to interpret observed actions. We suggest that, with natural human movement stimuli, motor representations contribute to action comprehension each time visual information is incomplete or ambiguous.

Keywords:

• Action comprehension
• Neural simulation
• Mirror neurons
• Embodied cognition
• Point-light animations
• Upper limb aplasia

We are very grateful to Simone Bosbach who kindly provided us with the material of Experiments 5 and 6. We thank Marcel Brass, Martin G. Edwards, and Richard Ramsey for their helpful comments on a previous draft of this paper. We obtained the motion capture database from mocap.cs.cmu.edu. (database created with funding from NSF EIA-0196217) and Christian van Brussel built the application used to generate point-light animations from this database.

This research was supported by a Fonds National de la Recherche Scientifique (FNRS) grant [grant number 1.5.192.10F] to Agnesa Pillon.

Notes

¹ The prediction tested in this study applies to theories of action comprehension based on a mechanism that maps directly the perceived movements onto the perceiver's own motor representation of the same or similar movements (Blakemore & Decety, 2001; Jeannerod, 2001; Rizzolatti et al., 2001). Recent formulations of the “mirror neurons” theory (e.g., Rizzolatti & Sinagaglia, 2010) moved away from this view by emphasizing the importance of a class of mirror neurons (so-called “broadly congruent mirror neurons”) that would directly map the goal of a perceived action onto the goal of an action in the perceiver's repertoire, regardless of whether the effector and movements are similar or different. We did not consider this hypothesis in the present study. It is unclear how a mechanism of direct execution–observation matching can operate when there are no motor characteristics in common between the motor plans involved in execution and the perceived motor act, and we are not aware of any attempt at describing how such a mechanism might work. One possibility that comes to mind is to suppose that “broadly congruent mirror neurons” in fact indirectly activate after the goal of the perceived action has been understood (by some other mechanism), in which case the mirror activity would be the consequence and not the means of action comprehension (for a similar view, see Csibra, 2007).

² Unfortunately, it is unknown whether apraxic patients who were not impaired in identifying pantomimes would show difficulties in identifying point-light animations of actions and, as a corollary, whether plegic patients would show no difficulty in identifying pantomimes—this should be examined in future studies.

³ A reviewer asked whether D.C. may not have acquired upper limb motor representations on the basis of visual experience alone. Although studies with aplasic individuals provide some evidence against this conjecture (e.g., Gazzola et al., 2007; Reilly & Sirigu, 2011; Stoeckel, Seitz, & Buetefisch, 2009), one cannot formally rule out that the mere observation of upper limb movements performed by others could lead to the formation of memory traces in the premotor/motor cortex of an individual unable to perform these movements due to a congenital absence of upper limbs. In any event, such memory traces cannot be considered as parts of a motor repertoire of upper limb actions—that is, a repertoire of means allowing the generation of motor programmes in order to achieve specific goals with the upper limbs. Let us give a reminder here that, according to motor theories of action comprehension (Blakemore & Decety, 2001; Jeannerod, 2001; Rizzolatti et al., 2001), the comprehension of an observed action is not driven by the activation of motor representations per se but by the activation of these representations as parts of a motor plan previously generated by the observer to achieve a specific goal. The observer understands the action by retrieving the goal he achieved when he previously performed similar movements. Thus, D.C. cannot be regarded as having a motor repertoire of manual actions, since he has never been able to achieve the goals of typically manual actions with his upper limbs.