Momentary reductions of attention permit greater 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.
References (36)
- et al.
Engrossed in conversation: the impact of cell phones on simulated driving performance
Accident Anal. Prev.
(2006) - et al.
Functional–anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI
Neuron
(1998) - et al.
Varieties of attention-deficit/hyperactivity disorder-related intra-individual variability
Biol. Psychiatry
(2005) - et al.
Working memory, comprehension, and aging: a review and new view
- et al.
Competition between functional brain networks mediates behavioral variability
NeuroImage
(2008) - et al.
Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing
NeuroImage
(2000) - et al.
Processing of irrelevant visual motion during performance of an auditory attention task
Neuropsychologia
(2001) - et al.
Behavior differences in drivers with attention deficit hyperactivity disorder: the driving behavior questionnaire
Accident Anal. Prev.
(2005) - et al.
FMRI studies of Stroop tasks reveal unique roles of anterior and posterior brain systems in attentional selection
J. Cogn. Neurosci.
(2000) - et al.
Sustained attention in mild Alzheimer's disease
Dev. Neuropsychol.
(2005)
Conflict monitoring versus selection-for-action in anterior cingulate cortex
Nature
Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging
Proc. Natl. Acad. Sci.
Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex
Proc. Natl. Acad. Sci. U. S. A.
Lapsing during sleep deprivation is associated with distributed changes in brain activation
J. Neurosci.
Modafinil for excessive sleepiness associated with shift-work sleep disorder
N. England J. Med.
Visual attention mediated by biased competition in extrastriate visual cortex
Philos. Trans. R. Soc. Lond., B Biol. Sci.
The human brain is intrinsically organized into dynamic, anticorrelated functional networks
Proc. Natl. Acad. Sci.
Statistical parametric maps in functional imaging: a general linear approach
Hum. Brain Mapp.
Cited by (38)
Enhancement of visual dominance effects at the response level in children with attention-deficit/hyperactivity disorder
2024, Journal of Experimental Child PsychologyReaction Time Variability in Children Is Specifically Associated With Attention Problems and Regional White Matter Microstructure
2023, Biological Psychiatry: Cognitive Neuroscience and NeuroimagingComponents of Motor Deficiencies in ADHD and Possible Interventions
2018, NeuroscienceCognitive persistence: Development and validation of a novel measure from the Wisconsin Card Sorting Test
2017, NeuropsychologiaCitation Excerpt :The aforementioned brain regions engaged during the WCST include cingulo-opercular regions that appear to serve as the neural instantiation of cognitive persistence. The cingulo-opercular network, consisting of the right and left IFG, anterior insula/frontal operculum (AIFO), and dACC, is upregulated when the task at hand becomes more difficult and/or performance drops (Botvinick et al., 2001, 2004, 1999; Carter, 1998; Crone et al., 2006; Durston et al., 2003; Eichele et al., 2008; Luks et al., 2007; Ridderinkhof et al., 2004; Weissman et al., 2006, 2009). Furthermore, cingulo-opercular engagement is associated with improved performance on the next trial (Botvinick et al., 2001, 2004; Kerns, 2006; Kerns et al., 2004; Orr and Weissman, 2009; Ridderinkhof et al., 2004; Weissman et al., 2006).