Neural correlates of attentional capture by unexpected sensory events: An event-related fMRI study

Abstract

Attentional capture by unexpected stimuli engages distinct neural pathways in the prefrontal and parietal cortex. We conducted event-related fMRI during a sustained attention task with intermixed novel distractors. BOLD signal increases in bilateral intraparietal sulcus and dorsolateral prefrontal cortex correlated with behavioural markers of attentional reorientation. Our findings suggest dissociable mechanisms for stimulus-driven versus goal-directed attention in healthy adults.

Introduction

Involuntary shifts of attention toward unexpected or task-irrelevant stimuli represent a fundamental aspect of human cognition. Previous behavioural and electrophysiological work has established that novel or salient events trigger rapid redirection of attentional resources, yet the large-scale neural networks supporting this process remain incompletely characterized. Understanding these mechanisms is critical for models of selective attention and for investigating how attentional control breaks down in clinical populations.

Recent advances in functional neuroimaging have enabled investigation of neural dynamics during attention-capturing events. Neuroimaging studies in non-human primates and human subjects using positron emission tomography have implicated the intraparietal sulcus and dorsal prefrontal regions. However, the temporal resolution afforded by these methods is limited. We hypothesize that event-related fMRI, with its superior temporal resolution relative to PET, will reveal fine-grained patterns of activation in these regions during attentional reorienting.

Method

Participants

Sixteen healthy volunteers (M age = 24.3 years, SD = 3.1; 8 female) with normal or corrected-to-normal vision participated. Participants reported no history of neurological or psychiatric disorder and were screened for contraindications to MRI. All provided written informed consent in accordance with institutional review board guidelines.

Procedure

Participants performed a sustained visual attention task during fMRI acquisition. On each trial, a sequence of four alphanumeric characters was presented centrally at 400 ms intervals. Participants monitored for the target letter X (p = 0.4). On 20% of trials, a sudden high-intensity white flash appeared in the peripheral visual field (outside the attended region) shortly after target onset. Task instructions emphasized maintaining focus on the central stream. fMRI data were acquired using a 3T Siemens Magnetom system with echo-planar imaging (TR = 2 s, TE = 30 ms, FOV = 22 cm, 3 mm isotropic voxels). A total of 360 volumes per participant were collected across three runs of 6 minutes each.

Results

Behavioural analysis revealed that unexpected peripheral flashes produced robust attentional capture: reaction times to targets presented in the 200-500 ms window following flash onset were elevated by approximately 85 ms relative to no-flash trials (M = 545 ms vs. M = 460 ms, t(15) = 4.2, p < 0.001). This effect was accompanied by a modest increase in error rates (3.2% vs. 1.8%, paired t(15) = 2.1, p = 0.052).

fMRI data were preprocessed using SPM5 (motion correction, normalization to Montreal Neurological Institute space, smoothing with 8 mm FWHM Gaussian kernel). Statistical parametric maps were generated using a general linear model with regressors for flash-present and flash-absent trials, convolved with the canonical hemodynamic response function. At p < 0.001 (uncorrected, cluster extent > 10 voxels), significant BOLD signal increases during flash-capture trials were observed in bilateral intraparietal sulcus (MNI coordinates: ±38, -52, 48; t = 4.8) and right dorsolateral prefrontal cortex (MNI: 42, 28, 38; t = 4.3). A regression analysis revealed that the magnitude of parietal activation was significantly correlated with individual differences in reaction time slowing (r = 0.61, p = 0.015).

Discussion

Our findings demonstrate that sudden sensory events engage dorsal attention networks in the intraparietal sulcus and dorsolateral prefrontal cortex, even when task instructions discourage such shifts. The correlation between parietal activation magnitude and behavioural attentional capture suggests that the degree of neural reorienting predicts the strength of the behavioural effect. This supports the hypothesis that these regions function as a flexible control system responsible for redirecting attention in response to salient, albeit task-irrelevant, events.

The laterality of the effects deserves comment. While the intraparietal sulcus activation was bilateral, the prefrontal effects were predominantly right-lateralized. Recent models propose that dorsolateral prefrontal cortex supports top-down attentional control, whereas right ventrolateral regions may be more involved in stimulus-driven reorienting. Our results suggest a more distributed organization, with both regions contributing to capture-related processing. Future work employing effective connectivity analysis may clarify the functional interactions among these regions.

References

Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 201–215.
Downing, P. E., Jiang, Y., Shuman, M., & Kanwisher, N. (2001). A cortical area selective for visual processing of the human body. Science, 293(5539), 2470–2473.
Katsuki, F., & Constantinidis, C. (2014). Bottom-up and top-down attention: Different processes and overlapping neural systems. Neuroscientist, 20(5), 509–521.
Kastner, S., & Ungerleider, L. G. (2000). Mechanisms of visual attention in the human cortex. Annual Review of Neuroscience, 23, 315–341.
Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25–42.
Yantis, S., & Jonides, J. (1990). Abrupt visual onsets and selective attention: Voluntary versus automatic allocation. Journal of Experimental Psychology: Human Perception and Performance, 16(1), 121–134.
Theeuwes, J. (1994). Perceptual selectivity for color and form. Perception & Psychophysics, 56(2), 202–215.