Abstract

The ability to maintain focus and avoid distraction by goal-irrelevant stimuli is critical for performing many tasks and may be a key deficit in attention-related problems. Recent studies have demonstrated that irrelevant stimuli that are consciously perceived may be filtered out on a neural level and not cause the distraction triggered by subliminal stimuli. However, in everyday situations, suprathreshold stimuli often do capture attention, but the neural mechanisms by which some stimuli rapidly and automatically trigger distraction remain unknown. Here, we investigated the neural basis of distraction by utilizing a particularly strong form of distractor: the abrupt appearance of a new object. Our results revealed a competitive relation between brain regions coding the locations of the target and the distractor, with distractor processing increasing and target processing decreasing, but only when the distractor was a new object; an equivalent luminance change to an existing object neither generated distraction nor affected target processing. Results also revealed changes in neural activity in intraparietal sulcus (IPS) and temporo-parietal junction (TPJ) that were unique to the new object distractor condition. The strongest relations between behavioral distraction and neural activity were observed in these parietal regions. Furthermore, participants who were less susceptible to distraction showed a more consistent, albeit more moderate, level of activity in IPS and TPJ. The present results thus provide new evidence regarding the neural mechanisms underlying distraction and resistance to it.

INTRODUCTION

The vast amount of input to our sensory systems far exceeds the limited capacity of higher-order cognitive and motor systems. Selecting information relevant to our current goals is thus critical for efficient task performance, and this selection process is made possible by mechanisms of attention. When these mechanisms fail, individuals may be overly distracted by irrelevant information and cognitive functioning can be impaired, as observed following brain damage (i.e., unilateral neglect syndrome), in developmental disorders (e.g., autism, ADHD), and in clinical populations (e.g., depression, schizophrenia) (Barkley, 1997; Cornblatt & Keilp, 1994). On the other hand, some individuals (e.g., trained meditators) have been found to have especially efficient attention mechanisms that allow them to reduce distraction (Slagter et al., 2007; Tang et al., 2007). Mechanisms of distraction may thus be an important link between enhanced versus impaired cognitive functioning in healthy and disease states, but the neural mechanisms of distraction are not yet well understood.

Recent studies have begun to investigate these mechanisms of distraction. Tsushima, Sasaki, and Watanabe (2006) found that there was a significant decrement in behavioral performance of a central task and that significant activity was evoked in regions coding the irrelevant distractor when it was below the threshold of conscious perception. When the potential distractor was suprathreshold, however, participants were able to inhibit its neural processing, and avoided being distracted from their central task. This result suggests that distraction is more easily avoided when participants are consciously aware of the irrelevant stimuli than when the irrelevant stimuli are below the threshold of consciousness. However, in everyday situations, people are very often distracted by suprathreshold stimuli. The potentially distracting stimulus in the Tsushima et al. study (i.e., coherent direction of moving dots amid a background of randomly moving dots) was not an especially powerful stimulus for capturing attention. On the other hand, the abrupt appearance of a new object has been shown to produce a uniquely strong capture of attention (Jonides & Yantis, 1988; Yantis & Jonides, 1984).

Yantis and Jonides (1984) demonstrated that a new object appearing in the visual field consistently captured attention relative to changes to existing objects in a visual search paradigm. Yantis and Hillstrom (1994) further showed that the strong capture by the appearance of a new object was not simply due to luminance changes. They found that new objects captured attention even when the object was equiluminant with the background, whereas a highly salient luminance increment alone (that did not create a new object) did not capture attention. The researchers proposed that the appearance of a new object resulted in the creation of a new object file that was especially potent in capturing attention. Other studies have confirmed that the abrupt appearance of the object is a critical factor for attentional capture, by showing that changes in color, luminance, or motion alone did not capture attention (Enns, Austen, Di Lollo, Rauschenberger, & Yantis, 2001; Hillstrom & Yantis, 1994; Jonides & Yantis, 1988). An electrophysiological study also provided further support for the special status of new objects, finding a central posterior positivity that was evoked uniquely by the appearance of a new object (Hopfinger & Maxwell, 2005). Although some studies have shown that the capture of attention by a new object may not be entirely automatic (e.g., contingent attentional capture; Folk, Remington, & Johnston, 1992), the appearance of a new object is one of the most potent stimuli for eliciting an involuntary shift of attention (Schreij, Owens, & Theeuwes, 2008).

Although numerous studies have thus investigated the capture of attention to new objects, the mechanisms by which these new objects cause distraction are not well understood. In the current study, we investigated the neural activity that underlies behavioral distraction by utilizing a new object distractor to trigger a decrement in performance of an ongoing task. We were specifically interested in comparing activity in brain regions representing target and distractor stimuli, as the interaction between these regions may be more critical in understanding the mechanisms of distraction than is the absolute activity in either region alone. If the neural basis of distraction is simply a sufficiently high level of neural activity in brain regions processing a distractor, then we may not observe a modulation of target activity in the present study. However, if distraction involves a more active inhibition of competing stimuli, then we should observe reduced activity in target processing regions when distraction is observed in behavior. Previous research has shown that voluntary attention can modulate the competitive biasing between stimuli, by reducing competition effects from other simultaneously presented stimuli (Kastner & Ungerleider, 2001; Moran & Desimone, 1985). However, some previous investigations of distraction failed to find evidence for a significant suppression of target processing, even in conditions where there was enhanced distractor processing (Serences & Yantis, 2007; Tsushima et al., 2006). Recent evidence suggests that target processing in visual regions may be suppressed when the distracting stimuli are potentially relevant (Geng et al., 2006). In the present study, we investigated the automaticity and generality of this mechanism by testing whether this suppression of target processing occurs when the distractor is known to be completely irrelevant and is highly distinct from the target in terms of features and spatial location.

In addition to visual processing regions, areas of the parietal and temporal lobes are also likely involved in distraction. Previous studies have suggested that intraparietal sulcus (IPS) may be the source of an attentional control signal that enhances activity within visual areas (Corbetta, Kincade, Lewis, Snyder, & Sapir, 2005; Vandenberghe, Gitelman, Parrish, & Mesulam, 2001; Hopfinger, Buonocore, & Mangun, 2000). IPS also shows a transient increase in activity associated with attentional shifts (Yantis et al., 2002), and this activity is enhanced following distractors that share target properties relative to distractors that do not share critical target features (Serences & Yantis, 2007). Here, we test whether this region can be triggered in a bottom–up manner, even when the distractor does not share any target properties. Another region, right temporo-parietal junction (TPJ), is regarded as one of the critical regions for attentional reorienting, when attention needs to be quickly oriented back to a target (Hahn, Ross, & Stein, 2006; Vossel, Thiel, & Fink, 2006; Corbetta et al., 2005; Kincade, Abrams, Astafiev, Shulman, & Corbetta, 2005; Serences et al., 2005; Peelen, Heslenfeld, & Theeuwes, 2004; Corbetta, Kincade, & Shulman, 2002). In the current study, we tested whether the task-irrelevant distractor would evoke activities in IPS and TPJ, and furthermore, whether these activities would be related to behaviorally measured distraction.

In the present study, we developed a novel task in order to test the neural basis of distraction by a new object. Participants had to make a discrimination judgment regarding the orientation of a red letter, “T,” presented overlying the fixation cross. The target rotated to a random new orientation every second, but, critically, it never disappeared throughout the run, thereby ensuring that the target itself would not have the property of “new object.” The distractor was a luminance change (increase or decrease) of a square region in the periphery. The distractor was located at a single, fixed area in the upper right visual field. Critically, we manipulated the type of distractor across two conditions, run in separate blocks of trials. In the “object condition,” the distractor square appeared or disappeared at random intervals. In the “luminance-only condition,” everything was identical to the object condition except that an outline box was continuously present at the location of the distractor as part of the standing background for that condition. The luminance changes were the same for each condition. Critically, our design thus allowed us to compare effects of luminance changes with or without the appearance of new objects. Finally, we examined why some individuals may more effectively avoid distraction, by comparing more- versus less-distractible participants.

METHODS

Participants

Twenty-five healthy, right-handed volunteers were recruited for this study and were paid $20 per hour. All participants reported being free from neurological and psychiatric disorders and had normal or corrected-to-normal vision. All gave informed consent prior to participation in the study, but were naïve with regard to the specific hypotheses being tested here. Four participants' data were not usable due to problems with data acquisition. Additionally, one participant was removed due to an abnormal pattern of behavior responses (average RTs were more than three standard deviations greater than the average RTs among all other participants). Thus, the final analyses included data from 20 participants (10 women; aged 19–31 years; average age = 25.19 years; SD = 3.45 years).

Task, Stimuli, Procedures

Each volunteer participated in one fMRI session, during which they performed our task in two different conditions: an object condition and a luminance-only condition (see Figure 1). Participants were instructed to maintain fixation upon a centrally located cross throughout each block. The target, which was presented overlapping the fixation cross, randomly changed its orientation every second. In both object and luminance-only conditions, participants performed a discrimination task regarding the orientation of the target, a red letter “T,” which was continuously present. Participants were asked to press the first button on the response pad with their right index finger, if the “T” was oriented in the horizontal or vertical direction (i.e., 0°, 90°, 180°, or 270°), and press the second button using their right middle finger when the letter was oriented in a diagonal direction (i.e., 45°, 135°, 225°, or 315°). Notably, the letter never disappeared throughout each block, thereby ensuring it did not have the property of a new perceptual object. The target letter was red and subtended a visual angle of 1.33° × 1.33°, centered on the fixation cross. For both conditions, the background color was gray [“Red, Green, Blue (RGB)” of “125, 125, 125”], and the color of the fixation cross was black.

Figure 1. 

Trial sequence for each condition. The duration of each frame is 1 sec, and the target letter changed orientation between each frame. “T1” refers to the target occurring simultaneously with the peripheral distractor; “T Baseline” refers to all other targets. “T1” and “T Baseline” are defined separately for each condition (“Object” and “Luminance-only”) and separately for each luminance type (“Increment” and “Decrement”). For example, “T1, Increment” refers to a target occurring simultaneously with a luminance increment distractor. The duration between successive luminance events was equally drawn from the durations 5, 6, 7, 8, or 16 sec. The luminance change in the location of the distractor is the same in both conditions, but the thin black outline remains on the screen for the entire duration of the block in the luminance-only condition. Note that only the “T1, Increment” event in the object condition results in the appearance of a new object. In the experiment, the target was red, but it is shown as white here.

Figure 1. 

Trial sequence for each condition. The duration of each frame is 1 sec, and the target letter changed orientation between each frame. “T1” refers to the target occurring simultaneously with the peripheral distractor; “T Baseline” refers to all other targets. “T1” and “T Baseline” are defined separately for each condition (“Object” and “Luminance-only”) and separately for each luminance type (“Increment” and “Decrement”). For example, “T1, Increment” refers to a target occurring simultaneously with a luminance increment distractor. The duration between successive luminance events was equally drawn from the durations 5, 6, 7, 8, or 16 sec. The luminance change in the location of the distractor is the same in both conditions, but the thin black outline remains on the screen for the entire duration of the block in the luminance-only condition. Note that only the “T1, Increment” event in the object condition results in the appearance of a new object. In the experiment, the target was red, but it is shown as white here.

In the object condition, a light gray square (3.66° × 3.66°; RGB = “153, 153, 153”) abruptly appeared or disappeared in the upper right visual field (5.17° above and 5.17° right from the center of fixation to the center of square) while participants were performing the target task. The duration that the square remained on the screen was pseudorandomly selected and counterbalanced throughout the experiment, as either 5, 6, 7, 8, or 16 sec. There were equal numbers of trials with each of these durations. The disappearance of the square also occurred for the durations of either 5, 6, 7, 8, or 16 sec, pseudorandomly selected to have equal frequency within a block. Participants were asked to ignore this gray square because it was irrelevant to the task that they were performing. In the luminance-only condition, the task and procedure were identical to those in the object condition, except that a thin black outline box was ever-present throughout all trials, at the location of the distractor.

Each participant performed six runs of each condition, and each run lasted 260 sec. Every two runs composed a mega-run, and each mega-run contained 420 target events.1 Each participant performed a practice block for each condition. Each practice block lasted for 1 min and consisted of 60 trials.

Functional Localizer Run

A separate, functional localizer run was conducted to identify the volumes of interest (VOIs) in visual cortex corresponding to the distractor square and to the central target. In the localizer run, participants were asked to fixate a centrally located red cross at all times, and a checkerboard was flashed either at fixation (corresponding to the location of the targets) or at the location of the square distractor in the upper right visual field. Each square of the checkerboard reversed contrast (black/white) at a frequency of 4 Hz for a duration of 16 sec, interposed with 16 sec of “blank” screen (i.e., only the red fixation cross was on the screen, ever-present throughout the localizer scans). The sequence of this run was: (1) central checkerboard, (2) fixation only, (3) peripheral checkerboard, (4) fixation only; this sequence was repeated six times. The duration of the localizer scan was 6 min and 24 sec.

Imaging Methods and Analyses

Image Acquisition

Functional images were acquired with a Siemens 3-Tesla Allegra head-only MRI scanner at the University of North Carolina's Biomedical Research Imaging Center. Each participant completed 13 functional runs (i.e., 12 experimental runs and a localizer run), along with an anatomical scan. Each brain volume was composed of 34 transverse slices (FOV = 243 × 243, matrix = 64 × 64, 3.8 × 3.8 × 3.8 mm resolution) aligned to the AC–PC line, collected interleaved, inferior to superior. These images were acquired using a T2*-weighted EPI sequence (TR = 2000 msec, TE = 30 msec, flip angle = 80°). In all functional runs, data from the first two volumes were discarded to allow for stabilization of magnetic fields. Each experimental run was 260 sec, and the localizer run was 388 sec. An anatomical scan was acquired for each participant using a T1-weighted MP-RAGE sequence (TR = 1700 msec, TE = 4.38 msec, flip angle = 8°, FOV = 280 × 320, 160 slices, matrix = 224 × 256, 1.25 × 1.25 × 1.25 mm resolution, 382 sec acquisition time).

Localizer and anatomical scans were interspersed with task runs to provide rest between the multiple task runs. The order of runs was: four runs of the task (two of each condition, or one “mega-run” of each condition), functional localizer, four more task runs (two of each condition), anatomical scan, and four more task runs (two of each condition). The order of task blocks was counterbalanced across participants. For all task and localizer runs, participants were asked to maintain fixation upon the central fixation cross, and they were aware that compliance was being monitored vigilantly on-line by the experimenter using a long-range optics camera (Applied Science Laboratories, Bedford, MA).

fMRI Data Analysis

Preprocessing

The data from functional scans were analyzed with the statistical parametric mapping (SPM2) software from the Wellcome Department of Imaging Neuroscience (Queen Square, London, UK), run within Matlab (Mathworks, Natick, MA). Data were slice-time corrected for acquisition order (referenced to the slice acquired in the middle of the time sequence), motion corrected with coregistration without reslicing via INRIalign (Freire & Mangin, 2001), spatially normalized (with trilinear interpolation and preserving the intensities of the original images) to the SPM2 EPI template corresponding to the Montreal Neurological Institute (MNI) defined standardized brain space, and spatially smoothed with a Gaussian kernel of 8 mm FWHM. The time series were high-pass filtered at 128 sec.

Statistical analyses

Contrast maps for the task runs were first estimated for each individual using an event-related hemodynamic response function time-locked to the luminance change of the peripheral square distractor for each condition. Consistent effects across participants were then tested by including these contrast images in one-sample t tests (conforming to random effects analyses) in order to make population inferences.

Because we had a priori regions of interest (i.e., target and distractor processing regions in occipital lobe, and higher-order attentional control areas), small volume correction (SVC) was used to assess significant activity in those regions. To correct for multiple comparisons, we used a family-wise correction (FWE) within each SVC region. The SVC regions for the target and distractor processing areas of visual cortex were defined as 4-mm spheres surrounding the maximum activity identified with the localizer scan. SVC for IPS was defined as a cubic region (MNI coordinates: x = 25 to 40; y = −76 to −60; z = 28 to 45) that encompassed activations labeled as right IPS in previous studies of attentional orienting (Ansari, Dhital, & Siong, 2006; Corbetta et al., 2005; Vandenberghe et al., 2001; Connolly, Goodale, Menon, & Munoz, 2002; Hopfinger et al., 2000; Wojciulik & Kanwisher, 1999). Similarly, SVC for TPJ was a cubic region (MNI coordinates: x = 45 to 61; y = −57 to −29; z = 8 to 30) that encompassed all the activations labeled as right TPJ in previous attention studies (Hahn et al., 2006; Vossel et al., 2006; Corbetta et al., 2002, 2005; Kincade et al., 2005; Serences et al., 2005; Peelen et al., 2004; Corbetta, Kincade, Ollinger, McAvoy, & Shulman, 2000). MarsBar software (http://marsbar.sourceforge.net; Brett, Anton, Valabregue, & Poline, 2002) was used to create the SVC mask regions.

Timecourse and peak activation analyses

VOI analyses were conducted using SPM2 and MarsBar software. Signal was extracted from all voxels within the VOI and averaged, and the peak of the response was tested. Two visual processing VOIs were defined from the localizer scan: one region corresponding to the location of the peripheral distractor (from the contrast: “Distractor localizer > Target localizer”; Figure 2A) and one region corresponding to the location of the central target (from the contrast: “Target localizer > Distractor localizer”; Figure 3A). The localizer run was analyzed as a blocked design with event onsets defined as the first stimulus of each type of block and “event duration” set to 16 sec. The regions were obtained with a random effects analysis of the localizer scan with family-wise-corrected (FWE) for whole brain (p < .05) to locate the maxima for each contrast described above. VOIs in the occipital region were created as spheres (4 mm radius) around the maxima for each of these visual processing regions. VOIs for the IPS and TPJ regions were also defined as 4-mm spheres, centered on the location of the maximal effect from the contrast where these activities were observed (Luminance increment > Luminance decrement in the object condition).

Figure 2. 

Distractor processing. (A) Distractor processing area in the left hemisphere as defined by the localizer run for Distractor localizer > Target localizer. Lingual gyrus, MNI (x, y, z) = −8, −84, −8, p < .05, FWE-corrected for whole-brain analysis. (B) Effect of luminance in the object condition (contrast of “Luminance increment > Luminance decrement”). Lingual gyrus, MNI (x, y, z) = −4, −87, −4; p < .05, FWE-corrected for whole brain. To better illustrate the extent of the activity, these maps have a more liberal threshold (p < .001, uncorrected). Maps are not masked. (C) Interaction of condition and luminance [contrast of “Object (Increment > Decrement) > Luminance-only (Increment > Decrement)”]. Lingual gyrus, MNI (x, y, z) = −4, −87, −8; p < .05, FWE-corrected for whole brain. Again, maps are not masked and the threshold is p < .001, uncorrected, to illustrate the extent of the activity. (D) Mean peak group BOLD response (6 sec poststimulus) for the distractor VOI in each event. This region showed significantly enhanced activity only following a luminance increment in the object condition. “*” denotes significant effects (p < .05).

Figure 2. 

Distractor processing. (A) Distractor processing area in the left hemisphere as defined by the localizer run for Distractor localizer > Target localizer. Lingual gyrus, MNI (x, y, z) = −8, −84, −8, p < .05, FWE-corrected for whole-brain analysis. (B) Effect of luminance in the object condition (contrast of “Luminance increment > Luminance decrement”). Lingual gyrus, MNI (x, y, z) = −4, −87, −4; p < .05, FWE-corrected for whole brain. To better illustrate the extent of the activity, these maps have a more liberal threshold (p < .001, uncorrected). Maps are not masked. (C) Interaction of condition and luminance [contrast of “Object (Increment > Decrement) > Luminance-only (Increment > Decrement)”]. Lingual gyrus, MNI (x, y, z) = −4, −87, −8; p < .05, FWE-corrected for whole brain. Again, maps are not masked and the threshold is p < .001, uncorrected, to illustrate the extent of the activity. (D) Mean peak group BOLD response (6 sec poststimulus) for the distractor VOI in each event. This region showed significantly enhanced activity only following a luminance increment in the object condition. “*” denotes significant effects (p < .05).

Figure 3. 

Target processing. (A) Target processing area in the right hemisphere as defined by the localizer run for Target localizer > Distractor localizer. Inferior occipital gyrus, MNI (x, y, z) = 30, −91, −8, p < .05, FWE-corrected for whole brain. (B) Effect of luminance in the object condition (contrast of “Object decrement > Object increment”). Inferior occipital gyrus, MNI (x, y, z) = 34, −91, −8; p < .005, FWE-corrected within the target region SVC. Maps are not masked and the threshold is p < .005, uncorrected, to illustrate the extent of the activity. (C) Mean peak group BOLD response (the average values of 6 and 8 sec poststimulus) in the target VOI. There is significantly reduced activity following a luminance increment compared to a luminance decrement in the object condition.

Figure 3. 

Target processing. (A) Target processing area in the right hemisphere as defined by the localizer run for Target localizer > Distractor localizer. Inferior occipital gyrus, MNI (x, y, z) = 30, −91, −8, p < .05, FWE-corrected for whole brain. (B) Effect of luminance in the object condition (contrast of “Object decrement > Object increment”). Inferior occipital gyrus, MNI (x, y, z) = 34, −91, −8; p < .005, FWE-corrected within the target region SVC. Maps are not masked and the threshold is p < .005, uncorrected, to illustrate the extent of the activity. (C) Mean peak group BOLD response (the average values of 6 and 8 sec poststimulus) in the target VOI. There is significantly reduced activity following a luminance increment compared to a luminance decrement in the object condition.

RESULTS

Behavioral Results

Responses faster than 150 msec or slower than 1150 msec were rejected from the analyses. To analyze accuracy data, we conducted a repeated measures ANOVA with three factors: condition (object/luminance-only), luminance type (increment/decrement), and target type (T1/T baseline). “T1” refers to the target occurring at the time of the peripheral luminance change, and “T baseline” refers to all other targets. In the three-way ANOVA, we found a significant main effect of target type [F(1, 19) = 7.779, p < .05], and a significant interaction between condition and luminance type [F(1, 19) = 5.924, p < .05]. The three-way interaction of condition, luminance type, and target type was also significant [F(1, 19) = 10.594, p < .05].

To further investigate the effects, we conducted separate two-way repeated measures ANOVAs for each condition. For the object condition, the ANOVA yielded a significant main effect of the luminance type [F(1, 19) = 10.079, p < .05] and of target type [F(1, 19) = 10.903, p < .05]. The interaction between luminance type and target type was also significant [F(1, 19) = 9.024, p < .05]. To examine whether the appearance or disappearance of a new object affected participants' performance on the central task, we conducted paired t tests for each event separately, and implemented the Benjamini–Hochberg (B–H) (1995) procedure to correct the alpha level in multiple comparisons using the false discovery rate. The mean accuracy for each event and significant effects from the paired t tests are shown in Table 1. In the object condition, the accuracy for responding to the T1 occurring simultaneously with the peripheral luminance increment (“T1, Increment”; M = 90.88) was significantly worse than the accuracy for “T Baseline, Increment” (M = 94.00) [mean differences (MD) = −3.12, t(19) = −5.02, p < .0001]. Moreover, the accuracy for “T1, Increment” was significantly worse than the accuracy for “T1, Decrement” [M = 94.14, MD = −3.26, t(19) = −3.27, p < .003]. For the luminance-only condition, neither main effects nor interaction was significant in the two-way ANOVA, and no pair revealed significant differences in the paired t test (Table 1).

Table 1. 

Behavioral Performance: Accuracy (Mean % Correct) and Response Time (msec)

Condition
Luminance
Accuracy
Response Times
T1
“T Baseline”
T1
“T Baseline”
Object Increment 90.88a,b (SD = 3.8) 94.00 (3.5) 527.1a,b (46.8) 510.2 (44.1) 
Decrement 94.14 (4.5) 93.96 (3.4) 512.5 (43.6) 515.8 (47.4) 
Luminance-only Increment 93.81 (4.3) 93.42 (3.7) 514.3 (46.6) 510.2 (46.1) 
Decrement 92.88 (4.5) 93.57 (3.8) 511.9 (50.3) 512.8 (48.6) 
Condition
Luminance
Accuracy
Response Times
T1
“T Baseline”
T1
“T Baseline”
Object Increment 90.88a,b (SD = 3.8) 94.00 (3.5) 527.1a,b (46.8) 510.2 (44.1) 
Decrement 94.14 (4.5) 93.96 (3.4) 512.5 (43.6) 515.8 (47.4) 
Luminance-only Increment 93.81 (4.3) 93.42 (3.7) 514.3 (46.6) 510.2 (46.1) 
Decrement 92.88 (4.5) 93.57 (3.8) 511.9 (50.3) 512.8 (48.6) 

Please see main text for complete statistics.

aDenotes significant accuracy differences versus T Baseline (significant after B–H correction for multiple comparisons).

bDenotes significant accuracy differences versus “T1, Decrement” (significant after B–H correction for multiple comparisons).

Analysis of RT showed that there was no speed–accuracy tradeoff, and confirmed the decrement in performance following the appearance of the new object distractor, as RTs were slower following this distractor event. The overall ANOVA revealed a significant three-way interaction of condition, luminance type, and target type [F(1, 19) = 9.024, p < .05]. Paired t tests (with B–H correction) revealed that RTs to the “T1, Increment” (M = 527.1 msec) were significantly slower than RTs to the “T Baseline, Increment” (M = 510.2 msec) [MD = 16.9, t(19) = 5.862, p < .0001] in the object condition. RTs to “T1, Increment” were also slower than RTs to the “T1, Decrement” (M = 512.5 msec) [MD = 14.6, t(19) = 3.941, p < .0005]. For the luminance-only condition, no pair revealed significant differences in the paired t test (Table 1).

fMRI Results

Distractor Processing Region

The localizer scan identified a region in left ventral occipital cortex (x, y, z: −8, −84, −8; Figure 2A) as showing the greatest activity for stimuli at the distractor location (p < .05, FWE-corrected for whole brain); the distractor VOI was centered on this location, with a radius of 4 mm. In the random effects analyses of the task runs, we found that this occipital activity was uniquely associated with the appearance of a new object. Specifically, only the contrast “Luminance increment > Luminance decrement” in the object condition showed significantly enhanced activity in the same region (p < .005, FWE-corrected for whole brain; Table 2 and Figure 2B); the same contrast in the luminance-only condition did not show any significant activation in the distractor-related occipital area (even at a more liberal p < .05, uncorrected threshold). Furthermore, we found significant Condition × Luminance interaction specified by the contrast “Object (Increment > Decrement) > Luminance-only (Increment > Decrement)” [p < .001, FWE-corrected for whole brain; MNI (x, y, z) = −4, −87, −8, Z = 4.73; Figure 2C]. These results suggest that change of luminance was processed differently depending on whether the event was defining a new object or not. The peak of the BOLD response within this VOI for each event type is plotted in Figure 2D. A two-way repeated measures ANOVA (Condition × Luminance) on this peak BOLD response confirmed the effects above, showing a significant interaction between condition and luminance [F(1, 19) = 11.961, p < .05]. This peak response was significantly greater for the new object event in the object condition compared to all other conditions: (1) greater than the luminance decrement event in the object condition [MD = 0.1925, t(19) = 4.091, p < .05]; (2) greater than the luminance increment in the luminance-only condition [MD = 0.1421, t(19) = 3.593, p < .05]; and (3) greater than the luminance decrement in the luminance-only condition [MD = 0.1147, t(19) = 2.910, p < .05]. Luminance increments and decrements in the luminance-only condition did not differ from each other [t(19) = −0.914, p = .37]. Finally, the increments and decrements in the luminance-only condition did not differ from the object decrement condition (all p > .1). Thus, activity in this distractor VOI was highly sensitive to the appearance of a new object, as was the case in behavioral measures of distraction.

Table 2. 

Activities in Each Region of Interest

Region
Contrast
K
Voxel
MNI
T
Z
p(unc)
p(FWE)
x, y, z {mm}
Distractor Obj_Inc > Obj_Dec 11 8.12 5.27 <.001 <.001 −4, −87, −4 
Target Obj_Dec > Obj_Inc 3.59 3.10 .001 .004 34, −91, −8 
R IPS Obj_Inc > Obj_Dec 4.01 3.37 <.001 .015 34, −76, 34 
R TPJ Obj_Inc > Obj_Dec 3.84 3.26 .001 .025 61, −46, 11 
Region
Contrast
K
Voxel
MNI
T
Z
p(unc)
p(FWE)
x, y, z {mm}
Distractor Obj_Inc > Obj_Dec 11 8.12 5.27 <.001 <.001 −4, −87, −4 
Target Obj_Dec > Obj_Inc 3.59 3.10 .001 .004 34, −91, −8 
R IPS Obj_Inc > Obj_Dec 4.01 3.37 <.001 .015 34, −76, 34 
R TPJ Obj_Inc > Obj_Dec 3.84 3.26 .001 .025 61, −46, 11 

K = size of cluster (number of contiguous voxels surviving the FWE-correction); p(unc) = uncorrected p value; p(FWE) = p value after family-wise error correction, using small volume correction (as described in Methods); Obj = object condition; Inc = increment; Dec = decrement.

Target Processing Region

The target VOI was centered on the occipital region showing the greatest activity in the localizer scan, from the contrast “Target localizer > Distractor localizer” (p < .05, FWE-corrected for whole brain); this was a region of ventral occipital cortex of the right hemisphere [MNI (x, y, z): 30, −91, −8; Figure 3A]. The random effects analyses for the object condition revealed a significant effect of luminance, as target processing was significantly diminished for luminance increments (i.e., onset of the new object) relative to luminance decrements (i.e., offset of the new object), p < .005, FWE-corrected, using SVC within the target processing region (Table 2 and Figure 3B). Such effect was not found in any contrasts in the luminance-only condition (all p > .05, uncorrected). These results thus suggest that only the appearance of a new object in the periphery is associated with reduced processing of the target stimuli. The analysis of the peak BOLD response in this target VOI for each event confirmed the significant reduction in activity for the increment event compared to the decrement event in the object condition [MD = −0.061, t(19) = −3.17, p < .05; Figure 3C]. In the luminance-only condition, there was no significant difference in luminance increments and decrements [MD = −0.018, t(19) = −0.51, p = .616].

Intraparietal Sulcus

Right IPS showed significant activity for the appearance of the new object event, as shown in the contrast “Luminance increment > Luminance decrement” in the object condition (p < .005, FWE-corrected, using SVC within IPS; Table 2 and Figure 4A). Importantly, there was no such boost of activity in IPS in any of the events in the luminance-only condition (all p > .05, uncorrected), confirming that the increased activity was associated with the appearance of the new object distractor. The analyses of the peak BOLD signal from this VOI (peak at 6 sec for the 4-mm-radius sphere around the maxima in IPS) confirmed these results, as there was significantly greater activity associated with the new object event compared to all other events (Table 3 and Figure 4C). These results thus suggest that the appearance of a new object is associated with increased activity in the IPS.

Figure 4. 

Activities in IPS and TPJ. (A) Activation of IPS for the contrast of “Object increment > Object decrement”; maximum effect for right IPS at MNI (x, y, z) = 34, −76, 34; p < .05, FWE-corrected within the IPS SVC. Maps are not masked and are shown at p < .005, uncorrected, to illustrate the extent of the activity. (B) Activation of TPJ for the contrast of “Object increment > Object decrement”; maximum effect for TPJ at MNI (x, y, z) = 61, −46, 11; p < .05, FWE-corrected within the TPJ SVC. Maps are not masked and are shown at p < .005, uncorrected, to illustrate the extent of the activity. (C) Mean peak group BOLD response (6 sec poststimulus) in the right IPS VOI. “*” denotes significant effects (p < .05). (D) Mean peak group BOLD response (6 sec poststimulus) in the right TPJ VOI. “*” denotes significant effects (p < .05).

Figure 4. 

Activities in IPS and TPJ. (A) Activation of IPS for the contrast of “Object increment > Object decrement”; maximum effect for right IPS at MNI (x, y, z) = 34, −76, 34; p < .05, FWE-corrected within the IPS SVC. Maps are not masked and are shown at p < .005, uncorrected, to illustrate the extent of the activity. (B) Activation of TPJ for the contrast of “Object increment > Object decrement”; maximum effect for TPJ at MNI (x, y, z) = 61, −46, 11; p < .05, FWE-corrected within the TPJ SVC. Maps are not masked and are shown at p < .005, uncorrected, to illustrate the extent of the activity. (C) Mean peak group BOLD response (6 sec poststimulus) in the right IPS VOI. “*” denotes significant effects (p < .05). (D) Mean peak group BOLD response (6 sec poststimulus) in the right TPJ VOI. “*” denotes significant effects (p < .05).

Table 3. 

Paired-sample t Tests for IPS and TPJ

Region
Pair
MD
t
df
p
R IPS Obj_Inc > Obj_Dec 0.098 2.28 19 .034 
Obj_Inc > Lumi_Inc 0.12 2.14 19 .045 
Obj_Inc > Lumi_Dec 0.13 2.33 19 .031 
R TPJ Obj_Inc > Obj_Dec 0.10 2.79 19 .012 
Obj_Inc > Lumi_Inc 0.12 2.47 19 .023 
Obj_Inc > Lumi_Dec 0.08 2.10 19 .049 
Region
Pair
MD
t
df
p
R IPS Obj_Inc > Obj_Dec 0.098 2.28 19 .034 
Obj_Inc > Lumi_Inc 0.12 2.14 19 .045 
Obj_Inc > Lumi_Dec 0.13 2.33 19 .031 
R TPJ Obj_Inc > Obj_Dec 0.10 2.79 19 .012 
Obj_Inc > Lumi_Inc 0.12 2.47 19 .023 
Obj_Inc > Lumi_Dec 0.08 2.10 19 .049 

Obj = object condition; Lumi = luminance-only condition; Inc = increment; Dec = decrement.

Temporo-parietal Junction

Activity in right TPJ was significantly enhanced following the appearance of a new object distractor in the object condition (p < .005, FWE-corrected, using SVC within TPJ; Table 2 and Figure 4B). For the luminance-only condition, activity did not approach significance for any contrast (all p > .05, uncorrected), confirming the significant role of new objects on activity in this region. Analysis of the peak BOLD responses in the TPJ VOI (peak at 6 sec for the 4-mm-radius spheres around the maxima in TPJ) confirmed that the activation in right TPJ was unique to the appearance of a new object, as there was a significant Task × Luminance interaction [F(1, 19) = 5.70, p < .05], and the onset of a new object distractor differed significantly from all other distractor events (Table 3 and Figure 4D).

Correlation Analysis between Behavior and Neural Responses

Above, we reported that occipital and parietal regions were uniquely activated during the condition showing behavioral distraction. To further assess the relation between these neural activities and distraction, we conducted correlation analyses. For the measure of brain activity, we used the VOIs described above (4-mm-radius sphere centered on the regional maxima in each of our a priori regions of interest: distractor area, target area, IPS, and TPJ). The parameter estimator (beta coefficient) for the contrast “Object luminance increment > Object luminance decrement” was then obtained within each VOI for each participant. For the behavioral distraction score, we calculated the difference between accuracy to the T1 target for the luminance increment event versus the luminance decrement event in the object condition (i.e., “luminance increment minus luminance decrement”). Greater distraction (worse performance on the task) is thus indexed by a smaller “accuracy distraction score.”

Somewhat surprisingly, the results revealed that behavioral distraction was not significantly correlated with activity in the target area (r = .331, p = .154) or the distractor area (r = −.178, p = .453). In contrast, there were significant correlations between behavioral distraction and neural activity in right IPS (r = −.470, p < .05) and right TPJ (r = −.445, p < .05). Combined with the lack of significant correlations in early visual regions, these data suggest that distractibility may have less to do with the absolute amount of early sensory processing of the distractor and the target, and more to do with the activity and efficiency of higher-order attentional control regions.

Comparison between More and Less Distractible Participants

To further investigate the neural activity underlying distraction, we divided our participants into two groups. Participants were ranked in terms of their accuracy distraction score, and divided into the 10 “more distractible” participants versus the 10 “less distractible” participants.2 The average distraction score for the more distractible group was −6.45 (range: −11.8 to −3.93), and the average for the less distractible group was −0.06 (range: −3.03 to 6.95). Two-sample t tests were conducted to examine if there were any group differences in brain activity in any of our critical regions. Both groups showed equivalent activation in the distractor and target VOIs [p > .05, uncorrected; in the contrast: Object luminance increment (i.e., new object) > Object luminance decrement]. However, in right IPS, the more distractible group showed significantly stronger activation than those with smaller distraction scores (x, y, z: 30, −72, 30; Z = 3.09, p < .05, FWE-corrected within the IPS VOI in the contrast: Object luminance increment > Object luminance decrement). Activation in right TPJ was also more enhanced in the more distractible group (x, y, z: 61, −49, 8; Z = 2.56, p < .05, FWE-corrected within the TPJ VOI). Although the more distractible group showed greater differential activity (appearance of a new object distractor > disappearance of the distractor) in IPS and TPJ, breaking down the effect further reveals a telling pattern. Less distractible participants showed a more consistent and moderate level of activity in IPS and TPJ, regardless of whether the object was appearing or disappearing (Figure 5). In contrast, more distractible participants showed very robust activity to a new object appearing, but no activity at all to its disappearance. This pattern of results is discussed more below.

Figure 5. 

Group analysis: More versus less distractible participants. (A) Mean peak group BOLD response (6 sec poststimulus) in the right IPS VOI in the object condition in each group. For the more distractible group (left), IPS activity was enhanced only in the luminance increment condition (i.e., new object). For the less distractible group (right), there was a consistent and more moderate level of activity for both luminance increment and decrement events. (B) Mean peak group BOLD response (6 sec poststimulus) in the right TPJ VOI in the object condition in each group. For the more distractible group (left), TPJ activity was enhanced only in the luminance increment condition (i.e., new object). For the less distractible group (right), there was a consistent and more moderate level of activity for both luminance increment and decrement events.

Figure 5. 

Group analysis: More versus less distractible participants. (A) Mean peak group BOLD response (6 sec poststimulus) in the right IPS VOI in the object condition in each group. For the more distractible group (left), IPS activity was enhanced only in the luminance increment condition (i.e., new object). For the less distractible group (right), there was a consistent and more moderate level of activity for both luminance increment and decrement events. (B) Mean peak group BOLD response (6 sec poststimulus) in the right TPJ VOI in the object condition in each group. For the more distractible group (left), TPJ activity was enhanced only in the luminance increment condition (i.e., new object). For the less distractible group (right), there was a consistent and more moderate level of activity for both luminance increment and decrement events.

GENERAL DISCUSSION

In the present study, we investigated distraction at behavioral and neural levels. Whether the capture of attention is completely automatic has been the subject of debate. Some research has suggested that capture is contingent on top–down control (e.g., Folk et al., 1992). Other results, however, have demonstrated that attention is initially captured involuntarily by the most salient feature or object in a display, regardless of one's top–down control settings, and only afterward is it oriented to the target (Schreij et al., 2008; Hickey, McDonald, & Theeuwes, 2006; Theeuwes, 1991a, 1992). Here, we found that participants could avoid distraction when the irrelevant, abrupt luminance change occurred in an already-existing object. These results are consistent with previous findings that individuals could inhibit a suprathreshold, task-irrelevant distractor when they were highly engaged in a central task (Tsushima et al., 2006). However, we found that the same luminance change could not be ignored when it created the appearance of a new object (i.e., in our “object condition”). Although the distractor appeared at a fixed peripheral location and did not share features with the target stimuli, the appearance of a new object resulted in significant distraction, as measured by poorer accuracy and slower responses on the main task.3 These results suggest that new objects capture attention and cause distraction even when the locations of the target and the distractor are known with complete certainty. This is in contrast to previous findings that failed to find capture by peripheral onsets when participants could anticipate the location of a target (Theeuwes, 1991b). Using a central cue and visual search paradigm, Theeuwes (1991b) found that a new object did not capture attention when a target location is precued by a central arrow. Further research may be necessary to resolve this difference, which may be due to differences in the structure of the tasks (our continuous performance task vs. visual search task) or in the nature of the onset stimuli (our task-irrelevant distractor concurrently presented with a target vs. an onset cue before the actual search display). Regardless, our within-subject results of distraction in one condition, but not another, allow us to isolate the neural activity related to distraction.

Corresponding to the behavioral indices of distraction, we found that the appearance of a task-irrelevant new object affected the neural processing of both the distractor and the target. Most previous neuroimaging studies of attentional capture have focused mainly on distractor processing and have either not reported target-evoked processing or have failed to find modulation of target processing caused by task-irrelevant distractors (Serences & Yantis, 2007; Tsushima et al., 2006; Schwartz et al., 2005). Recently, Geng et al. (2006) showed that distractors could modulate target processing. However, those distractors were task-relevant because they could potentially have been a target. Here, we demonstrated that the appearance of a new object not only enhanced activity in distractor processing regions but also significantly reduced activity in target processing regions, even though the distractor did not match the attentional set for the target stimulus.

Beyond visual processing regions, our analyses revealed that regions in the parietal and temporal lobes (i.e., IPS and TPJ) also showed increased activity related to the appearance of the new object distractor. These regions were found to be more strongly associated with behavioral measures of distraction than the visual processing regions. Furthermore, we found that participants who were less distractible engaged IPS and TPJ regardless of the status of distractor (e.g., new object onset or offset), whereas the more distractible participants only showed activity in response to the onset of a new object (summarized in Figure 6). This pattern would suggest that participants who efficiently engage these regions across all events may decrease distraction by lessening the involuntary capture to the new object, whereas participants who are not efficiently engaging these regions are more under the control of bottom–up factors. As indicated in Figure 6, bottom–up processing of the distractor did not differ significantly between groups. This provides evidence against the view that more distractible individuals simply have enhanced sensory processing that leads to capture and distraction. Instead, our results suggest that the processes supported by IPS and TPJ (disengaging attention, shifting, and reorienting attention) are the more critical elements in determining the degree of distraction suffered by individuals.

Figure 6. 

Summary figure. Top: Hypothesized mechanisms through trial sequence. Middle: Graphic representation of results for more versus less distractible participants during luminance increment trials in the object condition (i.e., new object onset). Small black circles represent inactivated regions, gray circles represent activated regions, and the size of the gray circle indicates the size of activation (e.g., larger circles representing greater activity). Bottom: Graphic representation of results for more versus less distractible participants during luminance decrement trials in the object condition (i.e., object offset). IPS = right hemisphere intraparietal sulcus; TPJ = right hemisphere temporo-parietal junction; D = distractor processing region in left visual cortex; T = target processing region in right visual cortex.

Figure 6. 

Summary figure. Top: Hypothesized mechanisms through trial sequence. Middle: Graphic representation of results for more versus less distractible participants during luminance increment trials in the object condition (i.e., new object onset). Small black circles represent inactivated regions, gray circles represent activated regions, and the size of the gray circle indicates the size of activation (e.g., larger circles representing greater activity). Bottom: Graphic representation of results for more versus less distractible participants during luminance decrement trials in the object condition (i.e., object offset). IPS = right hemisphere intraparietal sulcus; TPJ = right hemisphere temporo-parietal junction; D = distractor processing region in left visual cortex; T = target processing region in right visual cortex.

Recent studies on meditation may provide additional insight into the differences in distractibility that we observed. Those studies have shown that extensive meditation training can affect attentional performance and neural activity, especially in the frontal and parietal attentional control regions (Pagnoni, Cekic, & Guo, 2008; Brefczynski-Lewis, Lutz, Schaefer, Levinson, & Davidson, 2007; Slagter et al., 2007; Tang et al., 2007). In general, those findings suggest that meditation training initially results in increased activity in attentional control regions (relative to control subjects) but that after extensive practice, activity in these attentional control regions decreases below the level observed in control subjects. This latter result has been interpreted as improved efficiency of these attention networks, and this may fit with our finding that less distractible participants show less activity in IPS and TPJ than do more distractible participants, in the critical case when a new object distractor appears. Our less distractible participants may show better efficiency here because these participants utilize this same attention network more consistently, activating these regions even when the distractor is not especially salient (i.e., the offset of the object). In some forms of meditation training, the purpose is not to completely block out irrelevant stimuli or thoughts, but rather to register and acknowledge the sensation or thought, and then to disengage from that distraction and return to the focus of the meditation. This may relate to our results, in that IPS and TPJ may underlie this ability to register the distractor, disengage from it, and reorient back to the target task (Figure 6). Contrary to the idea that less distractible participants are better at inhibiting the initial processing of all potentially distracting stimuli, the present view would be that these individuals actually put more effort into processing the less salient distractors (e.g., object offset) and that the repeated engagement of the mechanisms of registration, disengagement, and reorienting leads to a better ability to avoid distraction when the distractor is highly salient (i.e., new object onset). More distractible participants, on the other hand, engage these attention systems only when it is most critical (i.e., new object onset), and thus, must work harder (greater IPS and TPJ activity) and are less efficient at these processes.

Although we have couched the present results in terms of the uniqueness of new objects, it remains difficult to separate whether the effects are specifically due to extra, enhanced processing of the new object (e.g., creation of a new object file) or due to the inhibition of preexisting stimuli, or if both mechanisms contribute to these effects. Previous research has shown that people can efficiently inhibit processing of preexisting objects. Watson and Humphreys (1997) demonstrated, in visual search tasks, that when one set of distractors is presented as a preview, participants are able to inhibit processing of these previewed items, an effect they termed visual marking. The visual marking phenomena suggest that individuals intentionally try to prioritize newly appearing stimuli and to ignore distracting but preexisting stimuli. Our results are, in part, congruent with findings in the visual marking literature. In our luminance-only condition, the distractor location was continuously demarcated by a standing box outline, and participants were able to inhibit the distractor in this condition, despite the change in its luminance. However, our paradigm and task are quite different from those in the visual marking paradigm. That is, the current study used a continuous performance task, and the distractor did not have any potential to be a target. Moreover, the location of the distractor was predetermined and did not change throughout the experiment. Thus, regardless of whether the distractor is an old object or not, intentional inhibition of the expected location of a distractor can be expected. Nonetheless, our new object distractor did gain attentional priority and impaired performance on the main task. This pattern thus tells us that there is extra processing of new object, relative to existing objects, even when the intention to ignore should be the same in each case.

In summary, our results provide new evidence that distraction involves both enhanced activity in distractor processing regions of visual cortex and significantly reduced activity in target processing regions. Furthermore, our results show that behaviorally measured distraction was most strongly related to the level of activity in the higher-order attentional regions, TPJ and IPS. Finally, our comparison of more versus less distractible participants suggests that consistent and efficient engagement of these attentional control regions may be critical for reducing distraction.

Acknowledgments

This work was supported by NIMH grant R01 MH066034 to J. B. H. We thank Kathy Wilber and Weili Lin for assistance with data collection and Emily Parks, Vicki Chanon, and Prerna Bholah for helpful and insightful comments.

Reprint requests should be sent to Joseph B. Hopfinger, Department of Psychology, University of North Carolina at Chapel Hill, CB 3270, Davie Hall, Chapel Hill, NC 27599-3270, or via e-mail: hopfinger@unc.edu.

Notes

1. 

To ensure that each block contained exactly equal numbers of each duration for each luminance event, we needed 420 targets to complete a block (i.e., the mega-block). However, given the intensive nature of the continuous performance task, we divided each mega-block in half and inserted a short rest period. Each half of the mega-block was a single fMRI run.

2. 

We are aware of the limitations of performing a median split analysis (e.g., reduces statistical power due to the reduction in the inherent variability of the predictor; MacCallum, Zhang, Preacher, & Rucker, 2002). Nevertheless, we believe that this analysis still provides important converging evidence for relations between behavioral distraction and neural activity.

3. 

The processing of peripheral distractors has been shown to be affected by attentional load (Lavie, 1995). Therefore, an open question is whether the appearance of a new object distractor in this paradigm could be ignored under stronger attentional focus. However, participants in the present study were able to inhibit processing of the luminance change in the luminance-only condition, under the same level of perceptual and attentional load as in the object condition. This suggests that the present task demands were strong enough to engage selective processing, and that the significant distraction was due to the appearance of the new object, not attentional load.

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