Applauding with closed hands: neural signature of action-sentence compatibility effects

Abstract

Background: Behavioral studies have provided evidence for an action-sentence compatibility effect (ACE) that suggests a coupling of motor mechanisms and action-sentence comprehension. When both processes are concurrent, the action sentence primes the actual movement, and simultaneously, the action affects comprehension. The aim of the present study was to investigate brain markers of bidirectional impact of language comprehension and motor processes.

Methodology/principal findings: Participants listened to sentences describing an action that involved an open hand, a closed hand, or no manual action. Each participant was asked to press a button to indicate his/her understanding of the sentence. Each participant was assigned a hand-shape, either closed or open, which had to be used to activate the button. There were two groups (depending on the assigned hand-shape) and three categories (compatible, incompatible and neutral) defined according to the compatibility between the response and the sentence. ACEs were found in both groups. Brain markers of semantic processing exhibited an N400-like component around the Cz electrode position. This component distinguishes between compatible and incompatible, with a greater negative deflection for incompatible. Motor response elicited a motor potential (MP) and a re-afferent potential (RAP), which are both enhanced in the compatible condition.

Conclusions/significance: The present findings provide the first ACE cortical measurements of semantic processing and the motor response. N400-like effects suggest that incompatibility with motor processes interferes in sentence comprehension in a semantic fashion. Modulation of motor potentials (MP and RAP) revealed a multimodal semantic facilitation of the motor response. Both results provide neural evidence of an action-sentence bidirectional relationship. Our results suggest that ACE is not an epiphenomenal post-sentence comprehension process. In contrast, motor-language integration occurring during the verb onset supports a genuine and ongoing brain motor-language interaction.

Figure 1. Response button and pre-assigned hand-shapes.

A) OH motor response during sentence comprehension task. B) CH motor response during sentence comprehension task. C) Custom-made response button. A commonly available USB joystick with analogue sticks was adapted to detect when a participant initiated a response.

Figure 2. RTs of ACE for OHG and CHG.

In the CHG, the compatible sequence trials comprised CHS and the incompatible comprised OHS. In the OHG, the compatible and incompatible effects were opposite. Vertical bars denote 0.95 confidence intervals.

Figure 3. N400-like effect for OHG and CHG.

The channel locations of selected electrodes are shown in the grey circle. Note that the incompatible stimuli which elicits N400 amplitude enhancement are OHS in CHG (Figure 3.A) and CHS in the OHG (Figure 3.B).

Figure 4. ERPs from motor responses.

A) Compatibility effects and difference waveforms for MP and RAP. B) Voltage maps from compatible and incompatible categories in the −100, 0 and 200 ms. C) Selected electrodes (Cz) showing compatibility effects in OHG and CHG. Channel locations are shown in the grey circle inside the figure.