The specificity of action knowledge in sensory and motor systems.

Christine E Watson,Bianca Bromberger,Eileen R Cardillo,Anjan Chatterjee

doi:10.3389/fpsyg.2014.00494

Abstract

Neuroimaging studies have found that sensorimotor systems are engaged when participants observe actions or comprehend action language. However, most of these studies have asked the binary question of whether action concepts are embodied or not, rather than whether sensory and motor areas of the brain contain graded amounts of information during putative action simulations. To address this question, we used repetition suppression (RS) functional magnetic resonance imaging to determine if functionally-localized motor movement and visual motion regions-of-interest (ROI) and two anatomical ROIs (inferior frontal gyrus, IFG; left posterior middle temporal gyrus, pMTG) were sensitive to changes in the exemplar (e.g., two different people “kicking”) or representational format (e.g., photograph or schematic drawing of someone “kicking”) within pairs of action images. We also investigated whether concrete versus more symbolic depictions of actions (i.e., photographs or schematic drawings) yielded different patterns of activation throughout the brain. We found that during a conceptual task, sensory and motor systems represent actions at different levels of specificity. While the visual motion ROI did not exhibit RS to different exemplars of the same action or to the same action depicted by different formats, the motor movement ROI did. These effects are consistent with “person-specific” action simulations: if the motor system is recruited for action understanding, it does so by activating one's own motor program for an action. We also observed significant repetition enhancement within the IFG ROI to different exemplars or formats of the same action, a result that may indicate additional cognitive processing on these trials. Finally, we found that the recruitment of posterior brain regions by action concepts depends on the format of the input: left lateral occipital cortex and right supramarginal gyrus responded more strongly to symbolic depictions of actions than concrete ones.

Highlights

A growing body of research suggests that our knowledge about the world is tightly intertwined with the brain’s systems for perception and action (Barsalou, 1999; Gallese and Lakoff, 2005; Decety and Grèzes, 2006; see Barsalou, 2008 for a review)
An absence of repetition suppression (RS) for changes in exemplar or format would be consistent with the hypothesis that sensory and motor simulations preserve instance-specific details about actions. In addition to these functional ROIs, we looked for RS within left posterior middle temporal gyrus and bilateral inferior frontal gyri (IFG), two areas of the brain consistently implicated in the representation of semantic knowledge of actions (e.g., Kilner et al, 2009; Kalénine et al, 2010)
We found a significant effect of action similarity [F(2, 28) = 28.7, p < 0.001] and a marginal effect of format type [F(2, 28) = 2.7, p = 0.08] (Figure 3A)

Summary

Introduction

A growing body of research suggests that our knowledge about the world is tightly intertwined with the brain’s systems for perception and action (Barsalou, 1999; Gallese and Lakoff, 2005; Decety and Grèzes, 2006; see Barsalou, 2008 for a review) On these “embodied” accounts of semantic memory, sensory and motor states from real-world experiences are re-activated, or simulated, when we understand the meaning of words or other symbols (Barsalou, 1999, 2003; Gallese and Lakoff, 2005). Action concepts may be represented within the same areas of the brain involved in executing and perceiving dynamic actions (see Watson et al, 2013 for a meta-analysis of this literature). (Throughout the manuscript, we will use “action concepts” as shorthand for “the semantic representations of actions”.)

Methods

Results

Conclusion