Elsevier

NeuroImage

Volume 48, Issue 3, 15 November 2009, Pages 609-615
NeuroImage

Momentary reductions of attention permit greater processing of irrelevant stimuli

https://doi.org/10.1016/j.neuroimage.2009.06.081Get rights and content

Abstract

Momentary reductions of attention can have extremely adverse outcomes, but it remains unclear whether increased distraction from irrelevant stimuli contributes to such outcomes. To investigate this hypothesis, we examined trial-by-trial relationships between brain activity and response time in twenty healthy adults while they performed a cross-modal selective attention task. In each trial, participants identified a relevant visual letter while ignoring an irrelevant auditory letter, which was mapped either to the same response as the visual letter (congruent trials) or to a different response (incongruent trials). As predicted, reductions of attention (i.e., increases of response time) were associated not only with decreased activity in sensory regions that processed the relevant visual stimuli, suggesting a failure to enhance the processing of those stimuli, but also with increased activity in sensory regions that processed the irrelevant auditory stimuli, suggesting a failure to suppress the processing of those stimuli. Reductions of attention were also linked to larger increases of activity in incongruent than in congruent trials in anterior cingulate regions that detect response conflict, suggesting that failing to suppress the sensory processing of the irrelevant auditory stimuli during attentional reductions allowed those stimuli to more readily activate conflicting responses in incongruent trials. These findings indicate that heightened levels of distraction during momentary reductions of attention likely stem, at least in part, from increased processing of irrelevant stimuli.

Introduction

Although often innocuous, momentary reductions of attention can have dire outcomes. For example, when experiencing a reduction of attention drivers take longer to step on the brake when an unexpected event occurs (Beede and Kass, 2006). Reductions of attention also profoundly disrupt behavior in numerous clinical syndromes, such as attention-deficit and hyperactivity disorder (ADHD) (Castellanos et al., 2005, Reimer et al., 2005), Alzheimer's disease (Berardi et al., 2005), and drug addiction (Hendricks et al., 2006). Understanding and minimizing reductions of attention therefore has tremendous theoretical and clinical importance.

Current models provide important clues as to which processes might be adversely affected by momentary reductions of attention. Specifically, they posit that attention facilitates performance not only by enhancing the processing of relevant stimuli, but also by limiting the processing of irrelevant stimuli (Desimone, 1998, Handy et al., 2001, Hasher and Zacks, 1988, Lavie et al., 2004). Thus, attentional reductions should both impair the processing of relevant stimuli and permit greater processing of irrelevant stimuli.

Using functional magnetic resonance imaging (fMRI), we recently investigated the effects of momentary reductions of attention on the processing of relevant stimuli in an intramodal visual selective attention task (Weissman et al., 2006). Natural variations in response time can serve as good dynamic markers of variations in attention (Castellanos et al., 2005). When a person experiences a reduction of attention, their responses to external stimuli become slower, and the degree of slowing depends on the severity of the reduction. Therefore, in our prior study we investigated the neural bases of momentary reductions of attention by correlating brain activity with response time (RT) on a trial-by-trial basis. Our findings provided strong evidence that reductions of attention (i.e., increases of RT) impair the processing of relevant stimuli. For example, reductions of attention were associated with reduced activity in sensory regions that processed behaviorally-relevant stimuli, suggesting that attention had failed to enhance the perceptual processing of those stimuli (Weissman et al., 2006).

In the present study, we used fMRI to investigate whether reductions of attention permit greater processing of irrelevant stimuli in a multisensory audiovisual selective attention task (Fig. 1). In each trial, participants identified a visual letter (X or O) while ignoring a simultaneously-presented auditory letter (X or O). The irrelevant auditory letter was equally likely to be congruent with the visual letter (i.e., both letters were Xs or Os; Fig. 1a), in which case the relevant and the irrelevant letters were mapped to the same response, or incongruent (i.e., one letter was an X, the other was an O; Fig. 1b), in which case the irrelevant letter was mapped to a different response than the relevant letter. Participants responded to the identity of the visual letter via a button press with either the left or the right thumb. Because low-level sensory aspects of visual and auditory stimuli are processed in mostly nonoverlapping regions of the cerebral cortex (Kandel et al., 2000), we were able to distinguish sensory activity for the irrelevant auditory letter from sensory activity for the relevant visual letter.

We made two predictions. First, we predicted that reductions of attention (i.e., increases of RT to correctly identify the relevant visual stimulus) would be associated not only with reduced activity in sensory regions that processed the relevant visual stimuli (Weissman et al., 2006), but also with increased activity in sensory regions that processed the irrelevant auditory stimuli. Second, we predicted that increased sensory processing of the irrelevant auditory stimuli during reductions of attention would allow those stimuli to more strongly activate the responses to which they were associated, thereby leading to greater conflict-related activity (i.e., activity that is greater in incongruent than in congruent trials) in anterior cingulate regions that detect response conflict (MacDonald et al., 2000, Weissman et al., 2004).

Section snippets

Participants

Twenty-two healthy participants (12 male, age range: 19–29, all right-handed) took part in the study. All had normal or corrected-to-normal vision with no history of serious neurological trauma or disorders. Furthermore, none reported any problems with their hearing. Two participants were excluded due to excessive head motion leaving twenty participants in the final analyses (10 male, age range: 19–29 years, all right-handed). Participants gave informed consent prior to the experiment in

Overall behavior

As expected, performance was significantly faster in congruent (482 ms), than in incongruent trials (500 ms), F(1,19) = 20.52, p < 0.001. Mean error rates in congruent (3.8%) and incongruent (4.2%) trials did not significantly differ, F(1,19) < 1.

fMRI

We posit that attention varies linearly and continuously as a function of response time, with the very fastest RT likely correlating with the most focused attention and the very slowest RT likely correlating with the least focused attention. From this

Discussion

Current models posit that attention serves not only to enhance the processing of relevant stimuli, but also to limit the processing of irrelevant stimuli (Desimone, 1998, Handy et al., 2001, Hasher and Zacks, 1988, Lavie et al., 2004). In the present study, we used an audiovisual selective attention task to conduct a novel investigation of this view, which involved determining whether momentary reductions of attention (i.e., increases of RT when correctly identifying relevant stimuli) are

Acknowledgments

This research was supported by NIH grants to D.H.W (1RO3DA021345-01) and to M.G.W. (R01-NS051048 and NSF-BCS-05-24031). We thank William Gehring, Patricia Reuter-Lorenz, Jerome Prado, and Joshua Carp for useful discussions and Kristina Visscher for useful discussions and helpful comments on an earlier version of this manuscript.

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