Research report
Performance degradation and altered cerebral activation during dual performance: Evidence for a bottom-up attentional system

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Abstract

Subjects performed a continuous tracking concurrently with an intermittent visual detection task to investigate the existence of competition for a capacity-limited stage (a bottleneck stage). Both perceptual and response-related processes between the two tasks were examined behaviorally and the changes in brain activity during dual-tasking relative to single-task were also assessed. Tracking error and joystick speed were analyzed for changes that were time-locked to visual detection stimuli. The associated brain activations were examined with functional magnetic resonance imaging (fMRI). These were analyzed using mixed block and event-related models to tease apart sustained neural activity and activations associated with individual events. Increased tracking error and decreased joystick speed were observed relative to the target stimuli in the dual-task condition only, which supports the existence of a bottleneck stage in response-related processes. Neuroimaging data show decreased activation to target relative to non-target stimuli in the dual-task condition in the left primary motor and somatosensory cortices controlling right-hand tracking, consistent with the tracking interference observed in behavioral data. Furthermore, the ventral attention system, rather than the dorsal attention system, was found to mediate task coordination between tracking and visual detection.

Introduction

Skilled performance typically requires executing multiple tasks simultaneously, many of which incorporate a continuous task in tandem with discrete tasks. For example, in driving, steering a vehicle is performed simultaneously with acceleration or braking. A consistent finding in dual-task studies, where subjects simultaneously perform two tasks, is the degradation of performance in one or both tasks relative to that observed for the single-task alone [4], [15], [21], [24], [28], [34], [43], [45]. Understanding the behavioral and the neural mechanisms underlying this degradation is essential to the safe performance of these skills, an important factor especially during vehicle operation. While numerous studies have examined dual-tasking with two overlapping discrete tasks behaviorally and with neuroimaging [8], [15], [28], [34], [39], [41], [44], studies combining behavioral with neuroimaging analyses to understand the effect of a continuous task simultaneously performed with a discrete task are still lacking. There is evidence that continuous tasks are divided into a series of discrete tasks, the scheduling of which may differ from executing discrete tasks alone [34], [47]. In well practiced subjects, van Mier et al. [47] found that motor execution for a previous move and motor planning for the next move overlapped in a continuous motor task. In continuous dual-tasking, the amount of interference was found to be dependent on the identity of the overlapping processing stages and was reduced when the retention stage of one task overlapped with the response stage of a second task relative to the interference during overlapping response stage in both tasks [17]. Thus, when a continuous task is performed simultaneously with a discrete task, the mechanism of dual-task interference may be distinct from that found in dual discrete tasks given the flexibility in task scheduling available to continuous tasks. The present study examined dual-tasking with a continuous task, compensatory tracking, and an intermittent task, visual detection, both behaviorally and with functional magnetic resonance imaging (fMRI) to determine the neural changes involved in dual-task interference.

Studies that have tested the effect of a simultaneous discrete task on continuous tracking have found performance decrement in one or both of tracking and the additional task [35]. For example, Griew [13] examined the effect of tracking concurrently with an auditory reaction time (RT) task. Subjects tracked with their left hand while responding to auditory signals with their right hand. Griew found a significant decrease in tracking performance as well as increases in RT relative to the corresponding measures in the single-task condition. Monty and Ruby [30] also found performance decrements in both tasks when tracking was executed simultaneously with a visual motor task. Netick and Klapp [31] reported changes in tracking behavior when concurrently performed with an auditory go/no-go task. Overall, tracking performance was consistently found to be degraded in the dual-task condition.

The sensorimotor processing in many motor tasks is understood to involve serial processing stages from initial perceptual states to final stages concerned with response programming and execution [29], [42]. For most tasks, the perceptual stages provide for stimulus detection and identification, and the response stages include selection and execution of the appropriate motor response. Performance degradation is attributed to limitation in the capacity of one or more stages shared between concurrent tasks, causing a bottleneck in the processing stream [8], [34]. Processing bottlenecks have been found for both perceptual [20] and response stages [32], [34]. Behaviorally, our study aimed to tease apart perceptual and response processes as the cause of performance degradation.

Both perceptual and response stages may be shared by the two tasks used in our study, compensatory tracking and visual detection, and might cause performance degradation [8]. In the current experimental design, visual stimuli for tracking were confined to the center of the screen while the detection stimuli resided in the periphery. Thus, saccades made to a peripheral detection stimulus from the central tracking field may be detrimental to tracking performance [9]. Deubel and Schneider [9] reported evidence for saccade to be indissociable from visual attention. In our study, saccade made to the detection stimuli may interfere with perception of the tracking cursor movement, and thus may underlie apparent competition for visual processing resources. As regards response processing, even though tracking was executed by the right hand and response to visual detection was made with the left, a common process may be responsible for generating motor instructions for both hands such that while instructions for one hand is processed, the other hand has to halt its movements until processing is completed for the first task.

In order to identify the bottleneck stage(s) shared by two concurrent tasks, previous studies manipulated different aspects of tasks, such as the stimulus onset asynchrony or the level of task difficulty, and measured changes in RT for both tasks [8], [21], [24], [33]. RT cannot readily be obtained in a continuous tracking task. To circumvent this difficulty we determined the changes in tracking error and movement speed that were time-locked to stimulus onset in the detection task. These variables quantify tracking behavior directly in terms of task performance and motor output, respectively. Thus, processing stages that experience dual-task interference can be identified by comparing trials that require specific stages of stimulus or response processing to ones that do not.

To control for stimulus processing required for the detection task, those same stimuli were also presented in the single-task tracking condition but subjects were told to ignore them. This manipulation maintained consistent visual stimulation between the single and the dual-task conditions and thus the main difference in processing stages between the non-targets in the two conditions was higher order perceptual processes. Increases in tracking error following non-target stimulus onset in the dual but not in the single-task condition would indicate a bottleneck in perceptual processing stages.

Response processing bottleneck would be revealed by changes in tracking error relative to the targets but that would not be observed for the non-target in the dual-task condition. Response-related processes were only active in target stimuli. Therefore, any changes associated only with target stimuli would reflect interference from response processes. If both perceptual and response processes contain processing bottleneck stages, then tracking error and joystick speed should show two periods of change during target stimuli and one period of change during non-target stimuli in the dual-task condition.

Neuroimaging studies of dual-tasking have reported two main types of effects. First, reduced dual-task activation relative to single-task regions were reported [12], [22], [23]. For example, Just et al. [23] compared brain activation in a driving simulation task when performed alone and while responding to true or false verbal questions. The authors reported decreased activation in the parietal lobe while performing both tasks relative to driving-only activation. The deactivation was likely due to interference from the verbal questions, reducing the amount of processing devoted to driving. Even though the interaction between tracking and visual detection in our study may cause brain activation changes different from that between driving and verbal processes, areas associated with tracking, such as the left primary motor and somatosensory cortices, should be affected similarly by a secondary task (i.e. decreased activation relative to single-task tracking).

The second effect seen in neuroimaging studies of dual-tasking is increased activation associated with the scheduling of two conflicting tasks [15], [39], [40], [41], [44]. Task order control is the assignment of priority to two simultaneous tasks for access to a bottleneck process. It becomes essential when conflict arises between two tasks and requires proportioning attention to the more immediate task, thus providing the task with access priority to the bottleneck stage. To locate brain regions associated with task order control, trials that need active task order control can be compared with those that only need passive control, such as task switching trials (active reversal of task order) relative to non-switch trials (same task order as previous trial) [44]. Any region that shows greater activation in the switch trials than the non-switch trials would be involved in task order control. Both Szameitat et al. [44] and Stelzel et al. [41] reported increased activation in the lateral prefrontal cortex to be associated with task scheduling. Alternatively, the intermittent appearance of detection stimuli may also trigger bottom-up attentional areas [6], drawing attention away from the primary task [27]. The bottom-up attention system differs from task order control in that it is externally motivated rather than guided by internal goals, thus it can replace the need for task order control in order to resolve dual-task conflict. Corbetta and Shulman [6] reported activation in the inferior frontal region to be part of the bottom-up attention system whereas the lateral prefrontal cortex is associated with active task scheduling in Szameitat et al. [44]. The pattern of frontal activation associated with a processing bottleneck stage in our result can elucidate the importance of each system in dual-tasking involving a continuous task.

To summarize we hypothesized that a bottleneck stage would produce: (a) increased tracking error time-locked to detection stimulus onset, (b) decreased joystick speed time-locked to detection stimulus onset, (c) decreased brain activation in areas mediating tracking performance, and (d) increased activation in the frontal cortex. Observation of these four effects would provide evidence of a bottleneck stage in the: (a) perceptual stages if the effects are found in the comparison between non-target stimuli in the single vs. the dual-task condition, and (b) response-related stages if the effects are found in dual-task target rather than non-target stimuli.

Section snippets

Participants

Two separate groups of subjects were included in the study. Both were tested under the same conditions, but the second group later participated in a sleep deprivation study. Behavioral and fMRI data for the second group were acquired before subjects were sleep deprived. All subjects were right-handed and screened to ensure that they had no history of medical, psychiatric, neurological, sleep disorder, or color-blindness. In group 1, 26 subjects were recruited but 4 had to be exclude (one

Behavioral data

Behavioral findings were analyzed in terms of trial means and of the means of binned data time-locked to detection stimulus onset. Trial means ANOVA tested the effects of Condition × Block × Trial × Group on the dependent variables tracking error, joystick speed, and false alarms, and for the dependent variables RT to target response and the number of correct responses, the effects were Block × Trial × Group. Binned means ANOVA for stimulus-locked tracking error and joystick speed contained the factors

Discussion

The goals of this study were to evaluate whether dual-task interference in continuous tracking results from bottleneck stages in the perceptual and/or response-related processes, and using fMRI to examine changes in brain activation when simultaneously performing a continuous and a discrete task.

Conclusion

Continuous tracking performed concurrently with a visual detection task caused degradation in tracking when response was made to target stimuli, consistent with a bottleneck stage in response processes. Decreased brain activity in the left primary motor cortex likely attributed to worsened tracking performance by decreasing the amount of error-correcting movement. Increased activation in regions associated with the bottom-up attention system suggests that conflict between the two tasks was

Acknowledgements

This work was supported by Army Research Office and the Defense Advanced Research Projects Agency for funding support (ARO and DARPA Grant DAAD19-02-1-0047). The views, opinions, and/or findings contained in this article/presentation are those of the author/presenter and should not be interpreted as representing the official views or policies, either expressed or implied, of the Defense Advanced Research Projects Agency or the Department of Defense. We thank Oksana Tatarina-Nulman, Linda

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