Elsevier

NeuroImage

Volume 40, Issue 1, 1 March 2008, Pages 298-307
NeuroImage

Selective attention modulates inferior frontal gyrus activity during action observation

https://doi.org/10.1016/j.neuroimage.2007.11.030Get rights and content

Abstract

Our ability to recognize the actions of others is subserved by a complex network of brain areas, including the inferior frontal gyrus (IFG), inferior parietal lobe (IPL) and superior temporal sulcus (STS). An unresolved issue is whether the activity within these regions requires top–down control or whether it arises relatively automatically during passive action observation. Here we used fMRI to determine whether cortical activity associated with action observation is modulated by the strategic allocation of selective attention. Participants observed moving and stationary images of reach-to-grasp hand actions, while they performed an attentionally demanding task at the fovea. We first defined regions-of-interest (ROIs) in the IFG, IPL and STS which responded to the perception of these actions. We then probed these ROIs while participants observed the identical, but now task-irrelevant, actions and instead performed an easy (low attentional load) or difficult (high attentional load) visual discrimination task. Our data indicate that the activity of the left IFG was consistently attenuated under conditions of high attentional load, while the remaining action observation areas remained relatively unaffected by attentional manipulations. The suppression of the left IFG was unique to the observation of hand actions, and did not occur during the observation of non-biological control stimuli, in the form of coherent dot motion. We propose that the left IFG is the site at which descending inhibitory processes affect the processing of observed actions, and that the attentional modulation of this region is responsible for filtering task-irrelevant actions during ongoing behavior.

Introduction

The human ability to recognize and interpret the actions of others is fundamental to communication and social perception. It is well established that action observation activates a complex network of brain areas, including the posterior inferior frontal gyrus (IFG, Brodmann's areas 44/45), the rostral inferior parietal lobe (IPL) and the superior temporal sulcus (STS) (Decety and Grèzes, 1999, Grèzes and Decety, 2001, Rizzolatti et al., 2001). The putative macaque homologues of these areas (ventral premotor area F5, inferior parietal area PF and the STS, respectively) contain cellular units which respond to biological actions, including goal-directed movements of the hand. In particular, a subpopulation of ‘mirror neurons’ in areas F5 and PF are sensitive to both the observation and the execution of reach-to-grasp hand actions (Gallese et al., 1996, Rizzolatti et al., 2001). Together, the activity of these areas is thought to be involved in the encoding and interpretation of observed gesture (Rizzolatti and Craighero, 2004).

Given the biological and human significance of action recognition, it has been postulated that perceived actions automatically recruit areas within the action observation network (Buccino et al., 2004, Coricelli, 2005, Gallese, 2003, Gallese et al., 1996, Rizzolatti and Craighero, 2004, Rizzolatti et al., 1996, Wilson and Knoblich, 2005). Current behavioral data from humans support the hypothesis that perceived actions are processed without the need for top–down control. For example, observing a goal-directed action typically facilitates the execution of the same, relative to a different movement (Brass et al., 2001, Brass et al., 2000, Craighero et al., 2002, Stürmer et al., 2000, Vogt et al., 2003), and may more generally prime movements involving the corresponding body part (Bach et al., 2007). These priming effects occur despite the observed action being task-irrelevant, which suggests that the processing of these actions cannot be suppressed, even if it is detrimental to task performance. Similar results have been found in studies that have recorded motor-evoked potentials (MEPs) from the extremities following transcranial magnetic stimulation (TMS) of primary motor cortex. These studies demonstrate that passively observing a hand movement results in MEPs in the corresponding arm and hand muscles of the participant, even though participants never themselves initiate a hand movement (Fadiga et al., 1995). Together, these results have been taken to suggest that observed actions are processed automatically and without conscious effort (Rizzolatti and Craighero, 2004, Wilson and Knoblich, 2005).

A hallmark of strongly automatic processes is that they operate without drawing on general cognitive resources, and that they are not subject to voluntary control (Pashler, 1998). If action observation is an automatic process, as implied by numerous behavioral observations, it should be relatively resistant to modulation by top–down mechanisms such as directed attention. This would be analogous to the operation of closely allied neural systems that are involved in the processing of biologically relevant stimuli. For example, amygdala activity in response to threat-related facial expressions persists even when participants' attention is directed toward a distractor stimulus (Vuilleumier et al., 2001, Williams et al., 2004) or is masked from awareness (Whalen et al., 1998). Such findings suggest that neural systems that evolved to extract the meaning and significance of biologically important stimuli, such as facial expressions, can influence behavior without the need for selective attention. Given the social importance of understanding the actions of others, it might be predicted that action observation areas in the brain would also be relatively immune to modulation by selective attention.

Clearly, however, there will be occasions when it is beneficial to suppress the processing of an observed action, especially if it is irrelevant or otherwise distracting. Consider, for example, being engaged in conversation with a colleague at a cocktail party, and having the distracting gestures of another guest fall within your line of sight. Here, selective attention is crucial to enhance the processing of behaviorally relevant stimuli – the sounds and lip movements made by the person to whom one is speaking – and to suppress the processing of the distracting gestures. Indeed, a recent behavioral study found that the visuomotor priming effects described earlier may only occur when the observed actions fall within participants' focus of spatial attention (Bach et al., 2007). This is consistent with the operation of several other perceptual systems, in which attention plays a crucial modulatory role (Lavie, 1995, Lavie, 2000). For example, neural signals associated with the perception of several classes of visual stimulus, including visual motion, faces and places, are reduced or even eliminated when participants are engaged in a separate task that involves a high attentional load (Pessoa et al., 2002, Schwartz et al., 2005, Yi et al., 2004).

Previous studies of the neural correlates of action observation in humans have used displays without a competing cognitive or perceptual load. Thus, the extent to which the activity within the action observation network is maintained under conditions of inattention is not known. If actions constitute a special class of stimuli with particular biological and social significance, neural activity associated with action observation should be unaffected by manipulations of attentional load. By contrast, if activity within action observation areas is constrained by the same processing bottleneck as other perceptual systems, as suggested by recent behavioral findings, then increasing the attentional load of a secondary task should attenuate this activity. Here we used fMRI to examine whether responses within human action observation areas can be modulated by selective attention during the observation of reach-to-grasp actions.

Section snippets

Participants

Sixteen right-handed, neurologically normal volunteers were recruited for this study. One participant was excluded based on a structural abnormality in his MRI scan. The remaining 15 participants (7 females) had an age range of 23–39 years (mean 27.3 years). All participants had normal or corrected-to-normal visual acuity. Volunteers were informed about potential risks and gave informed consent prior to entering the study. This study was approved by the ethics committees of St. Vincent's Health

Behavioral performance

Behavioral data verified the efficacy of the gap discrimination task in limiting participants' capacity to attend to the observed actions. A repeated measures ANOVA was conducted on participants' gap discrimination accuracy, with factors of Load (High vs. Low) and Session (Preliminary Session vs. Scanning Session). As expected, this analysis demonstrated that participants were less accurate in discriminating gap size in the High Load relative to the Low Load condition [F(1,14) = 149.152, p < 

Discussion

Our results demonstrate that the neural encoding of observed actions can be modulated by the intentional allocation of selective attention. Specifically, we found that activity within the left pars triangularis (BA 45) is reduced by having observers engage in an attentionally demanding task at the fovea. This effect manifested as a relative decrease in activity in this sector under conditions of High Load relative to Low Load. Critically, this difference in activity cannot be attributed to

Acknowledgments

The authors wish to thank Max Rademacher for technical assistance, as well as Mark Lourensz and St. Vincent's Health, Melbourne, for use of the MRI facilities. This research was supported by funds of the Howard Florey Institute, Melbourne, and by a University of Melbourne Grant to JBM, RC and MW. TC, RC and MW were supported by the National Health and Medical Research Council (NH and MRC) of Australia.

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