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Neural correlates of performance trade-offs and dual-task interference in bimanual coordination: An ERP investigation
Neuroscience Letters 400 (2006) 172–176
Neural correlates of performance trade-offs and dual-task interference in bimanual coordination: An ERP investigation Allison Matthews, Michael I. Garry, Frances Martin ∗ , Jeffery Summers School of Psychology, University of Tasmania, Australia Received 23 November 2005; received in revised form 15 February 2006; accepted 16 February 2006
Abstract Previous behavioural studies have provided a framework for understanding coordination dynamics using traditional dual-task methodology. The central cost associated with stabilising bimanual coordination patterns has been inferred from performance trade-offs during the concurrent performance of a probe reaction time (RT) task. The present study aimed to provide a direct measure of central cost by assessing electrophysiological correlates of performance trade-offs under dual-task conditions. Event-related potentials (ERPs) were recorded from 16 participants while an anti-phase bimanual coordination task and a visual three-stimulus task were performed under single task conditions and under dual-task conditions in which either task was prioritised. The visual task required a foot response to low probability target stimuli, while low probability distracter and high probability standard stimuli were ignored. Consistent with previous research, there was a performance trade-off between pattern stability and RT to visual targets when the coordination task was prioritised relative to when the visual task was prioritised. This was accompanied by a significant reduction in central P3a amplitude elicited by distracter stimuli and parietal P3b amplitude elicited by target stimuli. These findings indicate that prioritisation and thus stabilisation of the motor task reduced the amount of central/perceptual and automatic attentional resources available to perform the visual task providing insight into CNS mechanisms that constrain the coordination of movement through the allocation of attentional resources. © 2006 Elsevier Ireland Ltd. All rights reserved. Keywords: Bimanual coordination; Visual three-stimulus paradigm; Dual-task; Event-related potentials; Attentional resources
Two preferred behavioural patterns have been identified in bimanual coordination, the ‘in-phase’ pattern involving activation of homologous muscles and the ‘anti-phase’ pattern involving the activation of antagonist muscles [7]. Research has consistently shown that the anti-phase pattern is inherently less stable, such that spontaneous switches from anti-phase to in-phase coordination mode occur when oscillation frequency reaches a critical threshold. Energetic models of bimanual coordination argue that the less stable coordination patterns are more expensive in terms of “effort” or “energetic resources”, such that extra effort is required in order to maintain coordinative patterns against perturbing forces (see [20]). Attention is considered to be an important mediator of energetic resources [11] or effort [6] and is also an important mediating variable for the maintenance, stabilisation, and modification of behavioural coordination pat-
∗ Corresponding author at: School of Psychology, University of Tasmania, Private Bag 30, HOBART, Tasmania 7001, Australia. Tel.: +61 3 6226 2262; fax: +61 3 6226 2883. E-mail address: [email protected] (F. Martin).
0304-3940/$ – see front matter © 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2006.02.043
terns [10]. The amount of mental energy or effort allocated to a task is often referred to as attentional load and can be investigated using traditional dual-task methodology, such that a secondary task can be used as a probe to determine the amount of attentional resources required to preserve or improve performance on a primary task [21]. Recently, dual-task methodology has been applied in studies of interlimb coordination to investigate the relationship between coordination stability and attentional cost. Using a probe reaction time (RT) task Monno et al. [10] reported a covariation between coordination stability (relative phase variability) and central cost such that the most stable coordination modes were the least “expensive” to perform. Further, manipulation of attention by priority instructions has revealed performance trade-offs between coordination stability and central cost (probe RT), particularly for anti-phase coordination [20]. Resource theories argue that performance trade-offs reflect the competition for limited mental resources or processing capacity by the tasks being performed [6,23], whereas interference theories suggest that perturbations from one task to another result from the incompatible demands of concurrent activities
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on the same structure(s) and/or mechanism(s) [5]. Within this framework it has been argued that resource allocation, via priority instructions, may act to modify the stability of coordination selectively [20]. Multiple resource theory posits that dual-task interference occurs due to an overlap in resource pools related to processing stages (central, response), (visual, somatosensory), central codes (visual, spatial) or visual channels (focal, ambient) [23]. Although it is argued that probe RT indexes the central cost or attentional load associated with stabilising coordinative patterns [10], it is likely that RT includes the contribution of response related as well as central processes. The present study employs electroencephalography to provide a direct measure of the CNS activity associated with intentionally stabilising coordinative patterns during the concurrent performance of a visual three-stimulus paradigm. This paradigm involves the presentation of a standard high probability event, a low probability target deviant, and an equally low probability repeated distracter stimulus [8]. The target and distracter stimuli elicit the P3b and P3a components of the event-related potentials (ERP) waveforms, respectively. The P3b component elicited in response to low probability target stimuli is argued to index the allocation of central resources that are relatively independent of the processes of motor preparation and execution (see [8]). Although many studies have investigated the modulation of P3b amplitude under dual task conditions, to our knowledge, few studies have investigated the electrophysiological correlates of dual task performance during bimanual coordination. In contrast, the P3a component elicited by low probability distracter stimuli in a difficult target detection paradigm is shorter in latency and has a more fronto/central distribution than the P3b component. This P3a component is thought to be similar the P3a observed in response to ‘novel’ stimuli and may index a relatively automatic attentional switching mechanism that is associated with orienting towards novel and biologically relevant stimuli [1,14]. Few studies have investigated the modulation of P3a amplitude under dual task conditions. One study found no effect of a concurrent motor task on P3a amplitude to auditory targets [16], however, this study was designed to investigate habituation and fatigue and involved a uni-manual motor task. The present study investigated ERP correlates of central resource allocation during the concurrent performance of a visual three-stimulus and anti-phase bimanual coordination task. Based on previous findings [20], behavioural performance tradeoffs are expected under dual task conditions for both RT and accuracy to the visual target, and stability of bimanual coordination. These performance trade-offs are expected to be greatest for the visual task when the motor task is prioritised and vice versa. If central/perceptual resources are limited under dual-task conditions a reduction in P3b amplitude is expected, particularly when the coordination task is prioritised. A significant reduction in P3a amplitude may further indicate an overlap of automatic attentional resources by the two tasks being performed. Sixteen participants (8 M, 8 F), 18–27 years old (M = 20.28, S.D. = 2.58) were recruited on a voluntary basis from first year psychology students at the University of Tasmania. All participants gave written informed consent and completed a brief
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medical questionnaire prior to inclusion to the study. Participants were right handed as measured by the Edinburgh handedness inventory [12], with normal or corrected to normal vision. Exclusion criteria included a history of drug, alcohol, or tobacco abuse, psychiatric or neurological disorder, head trauma, seizure, and those currently receiving medication. Participants completed the National Adult Reading Test (NART) as a measure of general intelligence. NART raw scores ranged from 17 to 37 (M = 29.44, S.D. = 5.85). The study received approval from the Human Research Ethics (Tasmania) Network. For the bimanual coordination task, custom-built manipulanda in the form of inverted pendula served as handles and were grasped by participants to record pronation and supination movements of the forearm. Linear potentiometers (Bourns Instruments, Model No. 3540, 0.25%) were located coaxially with the axis of rotation of each handle (handle length 18 cm, handle diameter 2 cm) providing voltages that were converted to angular displacements. Output voltage signals were sampled at 200 Hz. The manipulanda were mounted on the table in front of the participant and could be adjusted to enable an elbow flexion of 90◦ . The visual three-stimulus task was presented visually using STIM software. Common (blue circle, 10.18 cm2 ), target (larger blue circle, 12.57 cm2 ), and distracter stimuli (large blue square, 20 cm2 ) were randomly presented with probabilities of .70 and .15, and .15, respectively. Distracter stimuli were used, rather than novel stimuli, to eliminate the variability associated with the presentation of truly novel stimuli. All stimuli were presented for 75 ms with an SOA of 1500 ms. The response window was 1000 ms. EEG activity was recorded from 32 electrode sites. A NeuroSCAN Synamps I system and Quik-cap with Ag/AgCl electrodes were used for data acquisition. Electrodes were referenced to linked mastoids and were grounded at AFz with impedances kept below 5 k. EEG activity was recorded with a bandpass filter of 0.15–100 Hz and digitized continuously at a rate of 1000 Hz. Vertical and horizontal EOG were recorded from electrodes above and below the left eye, and the outer can thus of each eye, respectively. Following set up for EEG recording, one-minute practice trials were conducted for the coordination and visual task separately and under dual task conditions. During practice trials, auditory pacing signals of 1.25 Hz were presented via a digital metronome. Auditory pacing was ceased during experimental trials and participants were asked to maintain movement frequency while producing synchronised, continuous anti-phase movements. Participants were instructed to respond as quickly and as accurately as possible to visual targets using a plantar flexion of the right foot and to ignore other stimuli. In the dual task conditions participants were asked to concentrate on the prioritised task. One five-minute trial of 200 visual stimuli, consisting of 30 target, 30 distracter, and 140 common stimuli, was run per condition. Four experimental trials were completed in counterbalanced order with brief rest periods between conditions. These were single visual (SV), single motor (SM), dual-task visual priority (DVP), and dual-task motor priority (DMP) conditions. All analyses were conducted in Statistica Version 7.0 using repeated measures ANOVA with Greenhouse Geisser correc-
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tions where appropriate. Where necessary, significant main effects and interactions were analysed using Tukey HSD post hoc tests. The displacement time-series data for the bimanual coordination task were low-pass filtered using a 10 Hz zero-phase shift Butterworth filter. Mean movement amplitude and frequency were calculated over the entire displacement time-series for each priority condition (SM, DMP, DVP). A custom peak-picking algorithm identified individual peaks and valleys in the timeseries. The frequency of individual cycles (peak-to-succeeding peak) and amplitude of individual half-cycles (peak-to-valley, valley-to-peak) were calculated and the individual frequencies averaged to obtain mean movement frequency and mean movement amplitude. Analyses of kinematic and coordination data were performed on 14 participants as data from two participants was discarded due to technical problems. To assess the effect of priority on kinematic performance a 3(Task: SM, DMP, DVP) × 2(Hand: left, right) within groups design was employed for both movement amplitude and frequency. There were no significant effects of Task or Hand for either dependent variable, indicating that movement kinematics were unaffected by changes of attentional priority. Estimates of continuous relative phase were obtained by rescaling each half-cycle (peak-to-valley, valley-to-peak) to the range [1,-1], resulting in a transformed displacement timeseries approximating a cosine function. Continuous phaseangles (degrees) for each arm were obtained by calculating the arccosine of each point and continuous relative phase was determined as the arithmetic difference in phase angles between the two limbs at each point [3]. The mean and S.D. of relative phase were calculated using circular statistics [9] over 1.5 s epochs preceding (pre) and following (post) the common stimuli under dual task conditions, and at matched epochs for the single task condition. The absolute deviation of mean relative phase from the required relative phase (180◦ ) was used as a measure of relative phase accuracy and the S.D. of relative phase was used as a measure of coordination stability. The effect of priority on relative phase accuracy and coordination stability were examined using a 3(Task: SM, DVP, DMP) × 2(epoch: pre, post) within groups design. Relative phase accuracy did not differ between dual-task and singletask conditions, F(2, 26) = .539, p > .05. However, analysis of coordination stability revealed a significant main effect of Task, F(2, 26) = 8.10, p < .01, such that stability was greater for the SM (9.2 ± 0.62 degrees) and DMP (9.9 ± 0.53 degrees) tasks compared with the DVP (11.7 ± 1.1 degrees) task. The reduced coordination stability of the DVP condition is consistent with the notion that maintenance of stability requires the allocation of attentional resources to the coordination task. To investigate the effect of bimanual coordination and attentional priority on probe RT and accuracy to the visual target stimulus a 3(Task: SV, DVP, DMP) within groups design was employed. To investigate the effect of task on peak amplitude and latency of P3a, and P3b components at midline electrodes (Fz, Cz, Pz) for the three conditions in which the visual task was completed, the following factor was incorporated, 3(Midline electrode: frontal, central, parietal).
The one-way ANOVA conducted on the RT to the target stimuli showed that there was a significant main effect of Task, F(2, 30) = 14.55, p < .001.Tukey HSD post hoc tests showed that RT was significantly greater for the DVP (M = 549, S.D. = .070) and DMP (M = 581, S.D. = .066) conditions compared to the SV condition (M = 515, S.D. = .071) and that RT was significantly greater when attention was allocated to the coordination task (DMP) than when attention was allocated to the visual task (DVP) (ps < .05). The one-way ANOVA conducted on the accuracy data also indicated a significant main effect of Task for the mean number of correct target detections, F(2, 30) = 6.47, p < .05. Tukey HSD post hoc tests indicated that accuracy was significantly lower for the DMP (M = 23.31, S.D. = 5.57) in comparison to both the SV (M = 26.38, S.D. = 4.03) and DVP (M = 25.75, S.E.M. = 1.22) conditions (ps < .05). EEG data were edited using SCAN 4.3 software. Continuous EEG files were merged with behavioural files and low pass filtered (30 Hz, 24 dB roll-off). Ocular artefact reduction was performed by regression and artefact averaging [17]. Stimuluslocked ERPs were epoched offline over 1100 ms, commencing 100 ms before stimulus onset. High and low voltage cut-offs for artefact rejection were 100 and −100 V. Correct responses were baseline corrected at the pre-stimulus interval. ERPs were averaged for common, target, and distracter stimuli and peak amplitude and latency were determined from grand mean averages and individually derived within the following intervals: P3b (300–600 ms), P3a (250–420 ms). Fig. 1a shows grand mean averaged ERP waveforms in response to distracter stimuli for each task condition. P3a amplitude and latency were analysed with a two-way (Task × Midline electrode) ANOVA. The main effect of Task was significant for P3a amplitude, F(2, 30) = 24.76, p < .001. Tukey HSD post hoc tests indicated that P3a amplitude was greater for the SV (M = 19.49, S.E.M. = 2.14) in comparison to both the DVP (M = 12.75, S.E.M. = 1.36) and DMP (M = 10.19, S.E.M. = 0.95) conditions (ps < .05). The main effect of Midline electrode was also significant, F(2, 30) = 7.65, p < .01, with Tukey HSD post hoc tests indicating that mean P3a amplitude was significantly greater at Cz (M = 15.55, S.E.M. = 1.53) in comparison to Pz (M = 12.95, S.E.M. = 1.52), but did not differ significantly from Fz (M = 13.93, S.E.M. = 1.12) (ps < .05). These main effects were qualified by a significant Task × Midline electrode interaction, F(4, 60) = 7.16, p < .01. Tukey HSD post hoc tests indicated that at all midline electrodes, P3a amplitude was significantly greater for the SV in comparison to both the DVP and DMP conditions and significantly greater for the DVP in comparison to the DMP condition (ps < .05). There were no significant effects involving task for P3a latency. Analyses across hemispheres did not show any theoretically significant results. Fig. 1b shows grand mean averaged ERP waveforms in response to target stimuli for each experimental condition. The two-way ANOVA conducted on P3b amplitude showed that the main effect of Task was not significant. The main effect of Midline electrode was significant, F(2, 30) = 24.03, p < .001, and Tukey HSD post hoc test showed that mean P3b amplitude was significantly greater at Pz (M = 12.33, S.E.M. = 1.14) in comparison to Cz (M = 8.70, S.E.M. = 8.70) and Fz (M = 6.60,
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Fig. 1. Grand mean averaged waveforms for distracter (a) and target (b) stimuli under SV, DVP and DMP conditions.
S.E.M. = .876), respectively (ps < .05). The Midline electrode × Task interaction was also significant, F(4, 60) = 3.20. Tukey HSD post hoc tests indicated that at parietal (Pz) and central (Cz) midline electrodes, P3b amplitude was significantly greater for the SV in comparison to the DMP condition (ps < .05). There were no significant differences between Tasks at Fz (ps > .05). When P3b latency was analysed using a two-way ANOVA, neither main effect was significant, but the Task × Midline electrode interaction was significant, F(4, 60) = 2.94, p < .05. Tukey HSD post hoc tests indicated that at Cz, P3b latency for the DMP condition (M = 435.9, S.E.M. = 22.83) was significantly longer in comparison to the SV condition (M = 414.0, S.E.M. = 20.15) (p < .05), but not significantly different to the DVP condition (M = 441.5, S.E.M. = 22.29). Again, analyses across hemispheres did not show any theoretically significant results. Relative to the SV task, there was a significant increase in RT for both dual task conditions indicating an overall dual task effect. Compared to the SM condition, there was a significant reduction in pattern stability for the DVP condition. However, there was no significant difference in pattern stability between the SM task and the DMP task, indicating that attention to the motor task prevented a loss of coordination stability under dual task conditions. This was also accompanied by a significant increase in RT relative to the DVP condition, representing the central cost associated with stabilising the coordination pattern. It could be argued that loss of stability occurred due to structural interference from discrete responses to the visual task however stability was measured pre and post common stimuli, which did not require an overt response. The only difference between the two dual task conditions was the attentional priority allocated to each task. The above prioritisation effects are in line with previous behavioural research investigating performance trade-offs under divided attention relative to attentional priority conditions using a probe RT [20]. However, due to the need to minimise fatigue and learning effects and maximise the number of low probability target stimuli for analysis, a divided attention control condition was not included in the current study. Although this prevents the dissociation of the relative effects of attention to the visual or motor task under dual-task conditions, the reductions in dual-task performance relative to single task performance when
attention is directed to either task indicates that attention was successfully manipulated and allows adequate assessment of the relative influence of attentional priority. The pattern observed in the behavioural data when the motor task was prioritised relative to when the visual task is prioritised is consistent with previous research in which performance trade-offs due to central cost (reduced stability and increased probe RT) have been observed as a function of priority [19]. Although it is argued that probe RT indexes the central cost or attentional load associated with stabilising coordinative patterns [10], it is likely that RT includes both central and response related resources and thus it may not be possible to completely dissociate these processes from behavioural measures alone. The P3b and P3a components are considered to index the allocation of central/perceptual and automatic attentional resources that are relatively independent of the resources associated with response preparation or execution (see [8,15]). In the present study P3a amplitude elicited by distracter visual stimuli was maximal at fronto-central midline electrodes, suggesting that the distracter stimulus elicited a P3a similar to that typically observed by novel stimuli [1,2]. There was an overall significant reduction in P3a amplitude under both dual task conditions relative to the single task condition, suggesting an overlap of a limited resource by the two tasks being performed [22,23] and a reduction in resources available for the automatic classification of distracter stimuli within the context of the visual task. However, there was also a significant reduction in P3a amplitude for the DMP relative to the DVP condition suggesting an additional reduction in automatic attentional resources available to evaluate distracter stimuli when attentional resources are allocated to the coordination task. These findings are not likely to be related to a reduction in response related resources as the distracter visual stimuli did not require an overt response. It has been suggested that the P3a component, when fronto-centrally maximal, reflects automatic attentional control mechanisms mediated by the frontal attentional network and may be related to working memory processes [13]. At central and parietal electrodes, prioritisation of the motor task resulted in a reduction in P3b amplitude relative to the single task condition. This is consistent with previous research finding a graded decrease in P3b amplitude as a function of attentional priority [18] and indicates a reduction in the cen-
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tral/perceptual resources available to perform the visual task. Considering that stability of coordination was maintained under this condition, P3b can be assumed to index the central cost associated with stabilisation of the coordination pattern [10]. When the visual task was prioritised, no reduction in P3b amplitude was found, despite a significant increase in RT relative to single task performance. This increase in RT, along with the decrease in coordination stability for this condition, may reflect an overall dual task effect due to the difficulty of the visual task. At the central electrode, prioritisation of the motor task also resulted in significant increase in P3b latency relative to the single visual task indicating an increase in stimulus evaluation time under these conditions. It has been suggested that the P3b component may index memory updating mechanisms subserved by temporal/parietal areas [13]. The present study was designed to investigate the electrophysiological correlates of the performance trade-off between coordination stability and central cost as a function of attentional priority [10]. The observed reduction in P3a amplitude under dual-task relative to the single task condition may indicate an overlap in resources related to the automatic attentional processing of stimuli by the two tasks being performed. The further reduction in P3a amplitude when the motor task was prioritised suggests that automatic attentional resources mediated by the frontal attentional network are also affected by the voluntary allocation of attention to the bimanual coordination task. The frontal attentional network (including areas such as the anterior cingulate gyrus (ACC), and lateral prefrontal cortex) has been shown to be involved in both complex motor control and the generation of P3a [4] and may be a possible locus for this effect. There was no loss of coordination stability under dual-task conditions in which the coordination task was prioritised and this was associated with an additional increase in RT, a decrease in parietal P3b amplitude, and an increase in central P3b latency to the visual target indexing the central cost of intentionally stabilising coordination under these conditions. Prioritisation of the visual task resulted in a significant reduction in both coordination stability and an increase in RT relative to single task conditions, though this was not accompanied by a significant reduction in P3b amplitude. The present study extends on previous research and demonstrates the utility of the P3b and P3a components for providing direct measures of the CNS activity associated with intentionally stabilising coordinative patterns. These indices allow insight into the types of resources or processes involved and are less likely to include the contribution of structural or response-related interference. Future research adopting this methodology may provide further insight into the relationship between coordination stability and central cost. Acknowledgment This work was supported by an ARC project grant (DPO451217) to the third and fourth authors.
References [1] M.D. Comerchero, J. Polich, P3a and P3b from auditory and visual stimuli, Clin. Neurophysiol. 110 (1999) 24–30. [2] D. Friedman, Y.M. Cycowicz, H. Gaeta, The novelty P3: an event-related brain potential (ERP) sign of the brain’s evaluation of novelty, Neurosci. Biobehav. Rev. 25 (2001) 355–373. [3] M.I. Garry, R.E. van Steenis, J.J. Summers, Interlimb coordination in stroke, Hum. Movem. Sci. 24 (2005) 849–864. [4] K.M. Hartikainen, R.T. Knight, Lateral and orbital prefrontal cortex contributions to attention, in: J. Polich (Ed.), Detection of Change: Event-Related Potential and fMRI Findings, Kluwer Academic Publishers, Dordnecht, Netherlands, 2003. [5] H. Heuer, Structural constraints on bimanual movements, Psychol. Rev. 55 (1993) 83–98. [6] D. Kahneman, Attention and Effort, Prentice-Hall, 1973. [7] J.A.S. Kelso, Phase transitions and critical behaviour in human bimanual coordination, Am. J. Physiol. 246 (1984) R1000–R1004. [8] A. Kok, Event-related-potential (ERP) reflections of mental resources: a review and synthesis, Biol. Psychol. 45 (1997) 19–56. [9] K.V. Mardia, Statistics of Directional Data, Academic Press, 1972. [10] A. Monno, J.J. Temprado, P.G. Zanone, M. Laurent, The interplay of attention and bimanual coordination dynamics, Acta Psychol. 110 (2002) 187–211. [11] D. Navon, Resources—a theoretical soup stone? Psychol. Rev. 91 (1984) 216–234. [12] R.C. Oldfield, The assessment and analysis of handedness: the Edinburgh inventory, Neuropsychologia 7 (1971) 97–113. [13] J. Polich, Theoretical overview of P3a and P3b, in: J. Polich (Ed.), Detection of Change: Event-Related Potential and fMRI Findings, Kluwer Academic Publishers, Dordnecht, Netherlands, 2003. [14] J. Polich, M.D. Comerchero, P3a from visual stimuli: typicality, task, and topography, Brain Topogr. 15 (2003) 141–152. [15] J. Polich, A. Kok, Cognitive and biological determinants of P300: an integrative review, Biol. Psychol. 41 (1995) 103–146. [16] M. Schubert, S. Johannes, M. Koch, B.M. Wieringa, R. Dengler, T.F. Munte, Differential effects of two motor tasks on ERPs in an auditory classification task: evidence of shared cognitive resources, Neurosci. Res. 30 (1998) 125–134. [17] H.V. Semlitsch, P. Anderer, P. Schuster, O. Presslich, A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP, Psychophysiology 23 (1986) 695–703. [18] D.L. Strayer, A.F. Kramer, Attentional requirements of automatic and controlled processing, J. Exp. Psychol.: Hum. Percept. Perform. 16 (1990) 67–82. [19] J.J. Temprado, A. Chardenon, M. Laurent, Interplay of biomechanical and neuromuscular constraints on pattern stability and attentional demands in a bimanual coordination task in human subjects, Neurosci. Lett. 303 (2001) 127–131. [20] J.J. Temprado, P.G. Zanone, A. Monno, M. Laurent, Attentional load associated with performing and stabilising preferred bimanual patterns, J. Exp. Psychol.: Hum. Percept. Perform. 25 (1999) 1579– 1594. [21] P.S. Tsang, T.L. Shaner, M.A. Vidulich, Resource scarcity and outcome conflict in time-sharing performance, Percept. Psychophys. 57 (1995) 365–378. [22] C.D. Wickens, Processing resources in attention, in: R. Parasuraman, D.R. Davies (Eds.), Varieties of Attention, Academic Press, San Diego, CA, 1984, pp. 63–98. [23] C.D. Wickens, Multiple resources and performance prediction, Theor. Issues Ergonom. Sci. 3 (2002) 159–177.
Neural correlates of performance trade-offs and dual-task interference in bimanual coordination: An ERP investigation Allison Matthews, Michael I. Garry, Frances Martin ∗ , Jeffery Summers School of Psychology, University of Tasmania, Australia Received 23 November 2005; received in revised form 15 February 2006; accepted 16 February 2006
Abstract Previous behavioural studies have provided a framework for understanding coordination dynamics using traditional dual-task methodology. The central cost associated with stabilising bimanual coordination patterns has been inferred from performance trade-offs during the concurrent performance of a probe reaction time (RT) task. The present study aimed to provide a direct measure of central cost by assessing electrophysiological correlates of performance trade-offs under dual-task conditions. Event-related potentials (ERPs) were recorded from 16 participants while an anti-phase bimanual coordination task and a visual three-stimulus task were performed under single task conditions and under dual-task conditions in which either task was prioritised. The visual task required a foot response to low probability target stimuli, while low probability distracter and high probability standard stimuli were ignored. Consistent with previous research, there was a performance trade-off between pattern stability and RT to visual targets when the coordination task was prioritised relative to when the visual task was prioritised. This was accompanied by a significant reduction in central P3a amplitude elicited by distracter stimuli and parietal P3b amplitude elicited by target stimuli. These findings indicate that prioritisation and thus stabilisation of the motor task reduced the amount of central/perceptual and automatic attentional resources available to perform the visual task providing insight into CNS mechanisms that constrain the coordination of movement through the allocation of attentional resources. © 2006 Elsevier Ireland Ltd. All rights reserved. Keywords: Bimanual coordination; Visual three-stimulus paradigm; Dual-task; Event-related potentials; Attentional resources
Two preferred behavioural patterns have been identified in bimanual coordination, the ‘in-phase’ pattern involving activation of homologous muscles and the ‘anti-phase’ pattern involving the activation of antagonist muscles [7]. Research has consistently shown that the anti-phase pattern is inherently less stable, such that spontaneous switches from anti-phase to in-phase coordination mode occur when oscillation frequency reaches a critical threshold. Energetic models of bimanual coordination argue that the less stable coordination patterns are more expensive in terms of “effort” or “energetic resources”, such that extra effort is required in order to maintain coordinative patterns against perturbing forces (see [20]). Attention is considered to be an important mediator of energetic resources [11] or effort [6] and is also an important mediating variable for the maintenance, stabilisation, and modification of behavioural coordination pat-
∗ Corresponding author at: School of Psychology, University of Tasmania, Private Bag 30, HOBART, Tasmania 7001, Australia. Tel.: +61 3 6226 2262; fax: +61 3 6226 2883. E-mail address: [email protected] (F. Martin).
0304-3940/$ – see front matter © 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2006.02.043
terns [10]. The amount of mental energy or effort allocated to a task is often referred to as attentional load and can be investigated using traditional dual-task methodology, such that a secondary task can be used as a probe to determine the amount of attentional resources required to preserve or improve performance on a primary task [21]. Recently, dual-task methodology has been applied in studies of interlimb coordination to investigate the relationship between coordination stability and attentional cost. Using a probe reaction time (RT) task Monno et al. [10] reported a covariation between coordination stability (relative phase variability) and central cost such that the most stable coordination modes were the least “expensive” to perform. Further, manipulation of attention by priority instructions has revealed performance trade-offs between coordination stability and central cost (probe RT), particularly for anti-phase coordination [20]. Resource theories argue that performance trade-offs reflect the competition for limited mental resources or processing capacity by the tasks being performed [6,23], whereas interference theories suggest that perturbations from one task to another result from the incompatible demands of concurrent activities
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on the same structure(s) and/or mechanism(s) [5]. Within this framework it has been argued that resource allocation, via priority instructions, may act to modify the stability of coordination selectively [20]. Multiple resource theory posits that dual-task interference occurs due to an overlap in resource pools related to processing stages (central, response), (visual, somatosensory), central codes (visual, spatial) or visual channels (focal, ambient) [23]. Although it is argued that probe RT indexes the central cost or attentional load associated with stabilising coordinative patterns [10], it is likely that RT includes the contribution of response related as well as central processes. The present study employs electroencephalography to provide a direct measure of the CNS activity associated with intentionally stabilising coordinative patterns during the concurrent performance of a visual three-stimulus paradigm. This paradigm involves the presentation of a standard high probability event, a low probability target deviant, and an equally low probability repeated distracter stimulus [8]. The target and distracter stimuli elicit the P3b and P3a components of the event-related potentials (ERP) waveforms, respectively. The P3b component elicited in response to low probability target stimuli is argued to index the allocation of central resources that are relatively independent of the processes of motor preparation and execution (see [8]). Although many studies have investigated the modulation of P3b amplitude under dual task conditions, to our knowledge, few studies have investigated the electrophysiological correlates of dual task performance during bimanual coordination. In contrast, the P3a component elicited by low probability distracter stimuli in a difficult target detection paradigm is shorter in latency and has a more fronto/central distribution than the P3b component. This P3a component is thought to be similar the P3a observed in response to ‘novel’ stimuli and may index a relatively automatic attentional switching mechanism that is associated with orienting towards novel and biologically relevant stimuli [1,14]. Few studies have investigated the modulation of P3a amplitude under dual task conditions. One study found no effect of a concurrent motor task on P3a amplitude to auditory targets [16], however, this study was designed to investigate habituation and fatigue and involved a uni-manual motor task. The present study investigated ERP correlates of central resource allocation during the concurrent performance of a visual three-stimulus and anti-phase bimanual coordination task. Based on previous findings [20], behavioural performance tradeoffs are expected under dual task conditions for both RT and accuracy to the visual target, and stability of bimanual coordination. These performance trade-offs are expected to be greatest for the visual task when the motor task is prioritised and vice versa. If central/perceptual resources are limited under dual-task conditions a reduction in P3b amplitude is expected, particularly when the coordination task is prioritised. A significant reduction in P3a amplitude may further indicate an overlap of automatic attentional resources by the two tasks being performed. Sixteen participants (8 M, 8 F), 18–27 years old (M = 20.28, S.D. = 2.58) were recruited on a voluntary basis from first year psychology students at the University of Tasmania. All participants gave written informed consent and completed a brief
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medical questionnaire prior to inclusion to the study. Participants were right handed as measured by the Edinburgh handedness inventory [12], with normal or corrected to normal vision. Exclusion criteria included a history of drug, alcohol, or tobacco abuse, psychiatric or neurological disorder, head trauma, seizure, and those currently receiving medication. Participants completed the National Adult Reading Test (NART) as a measure of general intelligence. NART raw scores ranged from 17 to 37 (M = 29.44, S.D. = 5.85). The study received approval from the Human Research Ethics (Tasmania) Network. For the bimanual coordination task, custom-built manipulanda in the form of inverted pendula served as handles and were grasped by participants to record pronation and supination movements of the forearm. Linear potentiometers (Bourns Instruments, Model No. 3540, 0.25%) were located coaxially with the axis of rotation of each handle (handle length 18 cm, handle diameter 2 cm) providing voltages that were converted to angular displacements. Output voltage signals were sampled at 200 Hz. The manipulanda were mounted on the table in front of the participant and could be adjusted to enable an elbow flexion of 90◦ . The visual three-stimulus task was presented visually using STIM software. Common (blue circle, 10.18 cm2 ), target (larger blue circle, 12.57 cm2 ), and distracter stimuli (large blue square, 20 cm2 ) were randomly presented with probabilities of .70 and .15, and .15, respectively. Distracter stimuli were used, rather than novel stimuli, to eliminate the variability associated with the presentation of truly novel stimuli. All stimuli were presented for 75 ms with an SOA of 1500 ms. The response window was 1000 ms. EEG activity was recorded from 32 electrode sites. A NeuroSCAN Synamps I system and Quik-cap with Ag/AgCl electrodes were used for data acquisition. Electrodes were referenced to linked mastoids and were grounded at AFz with impedances kept below 5 k. EEG activity was recorded with a bandpass filter of 0.15–100 Hz and digitized continuously at a rate of 1000 Hz. Vertical and horizontal EOG were recorded from electrodes above and below the left eye, and the outer can thus of each eye, respectively. Following set up for EEG recording, one-minute practice trials were conducted for the coordination and visual task separately and under dual task conditions. During practice trials, auditory pacing signals of 1.25 Hz were presented via a digital metronome. Auditory pacing was ceased during experimental trials and participants were asked to maintain movement frequency while producing synchronised, continuous anti-phase movements. Participants were instructed to respond as quickly and as accurately as possible to visual targets using a plantar flexion of the right foot and to ignore other stimuli. In the dual task conditions participants were asked to concentrate on the prioritised task. One five-minute trial of 200 visual stimuli, consisting of 30 target, 30 distracter, and 140 common stimuli, was run per condition. Four experimental trials were completed in counterbalanced order with brief rest periods between conditions. These were single visual (SV), single motor (SM), dual-task visual priority (DVP), and dual-task motor priority (DMP) conditions. All analyses were conducted in Statistica Version 7.0 using repeated measures ANOVA with Greenhouse Geisser correc-
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tions where appropriate. Where necessary, significant main effects and interactions were analysed using Tukey HSD post hoc tests. The displacement time-series data for the bimanual coordination task were low-pass filtered using a 10 Hz zero-phase shift Butterworth filter. Mean movement amplitude and frequency were calculated over the entire displacement time-series for each priority condition (SM, DMP, DVP). A custom peak-picking algorithm identified individual peaks and valleys in the timeseries. The frequency of individual cycles (peak-to-succeeding peak) and amplitude of individual half-cycles (peak-to-valley, valley-to-peak) were calculated and the individual frequencies averaged to obtain mean movement frequency and mean movement amplitude. Analyses of kinematic and coordination data were performed on 14 participants as data from two participants was discarded due to technical problems. To assess the effect of priority on kinematic performance a 3(Task: SM, DMP, DVP) × 2(Hand: left, right) within groups design was employed for both movement amplitude and frequency. There were no significant effects of Task or Hand for either dependent variable, indicating that movement kinematics were unaffected by changes of attentional priority. Estimates of continuous relative phase were obtained by rescaling each half-cycle (peak-to-valley, valley-to-peak) to the range [1,-1], resulting in a transformed displacement timeseries approximating a cosine function. Continuous phaseangles (degrees) for each arm were obtained by calculating the arccosine of each point and continuous relative phase was determined as the arithmetic difference in phase angles between the two limbs at each point [3]. The mean and S.D. of relative phase were calculated using circular statistics [9] over 1.5 s epochs preceding (pre) and following (post) the common stimuli under dual task conditions, and at matched epochs for the single task condition. The absolute deviation of mean relative phase from the required relative phase (180◦ ) was used as a measure of relative phase accuracy and the S.D. of relative phase was used as a measure of coordination stability. The effect of priority on relative phase accuracy and coordination stability were examined using a 3(Task: SM, DVP, DMP) × 2(epoch: pre, post) within groups design. Relative phase accuracy did not differ between dual-task and singletask conditions, F(2, 26) = .539, p > .05. However, analysis of coordination stability revealed a significant main effect of Task, F(2, 26) = 8.10, p < .01, such that stability was greater for the SM (9.2 ± 0.62 degrees) and DMP (9.9 ± 0.53 degrees) tasks compared with the DVP (11.7 ± 1.1 degrees) task. The reduced coordination stability of the DVP condition is consistent with the notion that maintenance of stability requires the allocation of attentional resources to the coordination task. To investigate the effect of bimanual coordination and attentional priority on probe RT and accuracy to the visual target stimulus a 3(Task: SV, DVP, DMP) within groups design was employed. To investigate the effect of task on peak amplitude and latency of P3a, and P3b components at midline electrodes (Fz, Cz, Pz) for the three conditions in which the visual task was completed, the following factor was incorporated, 3(Midline electrode: frontal, central, parietal).
The one-way ANOVA conducted on the RT to the target stimuli showed that there was a significant main effect of Task, F(2, 30) = 14.55, p < .001.Tukey HSD post hoc tests showed that RT was significantly greater for the DVP (M = 549, S.D. = .070) and DMP (M = 581, S.D. = .066) conditions compared to the SV condition (M = 515, S.D. = .071) and that RT was significantly greater when attention was allocated to the coordination task (DMP) than when attention was allocated to the visual task (DVP) (ps < .05). The one-way ANOVA conducted on the accuracy data also indicated a significant main effect of Task for the mean number of correct target detections, F(2, 30) = 6.47, p < .05. Tukey HSD post hoc tests indicated that accuracy was significantly lower for the DMP (M = 23.31, S.D. = 5.57) in comparison to both the SV (M = 26.38, S.D. = 4.03) and DVP (M = 25.75, S.E.M. = 1.22) conditions (ps < .05). EEG data were edited using SCAN 4.3 software. Continuous EEG files were merged with behavioural files and low pass filtered (30 Hz, 24 dB roll-off). Ocular artefact reduction was performed by regression and artefact averaging [17]. Stimuluslocked ERPs were epoched offline over 1100 ms, commencing 100 ms before stimulus onset. High and low voltage cut-offs for artefact rejection were 100 and −100 V. Correct responses were baseline corrected at the pre-stimulus interval. ERPs were averaged for common, target, and distracter stimuli and peak amplitude and latency were determined from grand mean averages and individually derived within the following intervals: P3b (300–600 ms), P3a (250–420 ms). Fig. 1a shows grand mean averaged ERP waveforms in response to distracter stimuli for each task condition. P3a amplitude and latency were analysed with a two-way (Task × Midline electrode) ANOVA. The main effect of Task was significant for P3a amplitude, F(2, 30) = 24.76, p < .001. Tukey HSD post hoc tests indicated that P3a amplitude was greater for the SV (M = 19.49, S.E.M. = 2.14) in comparison to both the DVP (M = 12.75, S.E.M. = 1.36) and DMP (M = 10.19, S.E.M. = 0.95) conditions (ps < .05). The main effect of Midline electrode was also significant, F(2, 30) = 7.65, p < .01, with Tukey HSD post hoc tests indicating that mean P3a amplitude was significantly greater at Cz (M = 15.55, S.E.M. = 1.53) in comparison to Pz (M = 12.95, S.E.M. = 1.52), but did not differ significantly from Fz (M = 13.93, S.E.M. = 1.12) (ps < .05). These main effects were qualified by a significant Task × Midline electrode interaction, F(4, 60) = 7.16, p < .01. Tukey HSD post hoc tests indicated that at all midline electrodes, P3a amplitude was significantly greater for the SV in comparison to both the DVP and DMP conditions and significantly greater for the DVP in comparison to the DMP condition (ps < .05). There were no significant effects involving task for P3a latency. Analyses across hemispheres did not show any theoretically significant results. Fig. 1b shows grand mean averaged ERP waveforms in response to target stimuli for each experimental condition. The two-way ANOVA conducted on P3b amplitude showed that the main effect of Task was not significant. The main effect of Midline electrode was significant, F(2, 30) = 24.03, p < .001, and Tukey HSD post hoc test showed that mean P3b amplitude was significantly greater at Pz (M = 12.33, S.E.M. = 1.14) in comparison to Cz (M = 8.70, S.E.M. = 8.70) and Fz (M = 6.60,
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Fig. 1. Grand mean averaged waveforms for distracter (a) and target (b) stimuli under SV, DVP and DMP conditions.
S.E.M. = .876), respectively (ps < .05). The Midline electrode × Task interaction was also significant, F(4, 60) = 3.20. Tukey HSD post hoc tests indicated that at parietal (Pz) and central (Cz) midline electrodes, P3b amplitude was significantly greater for the SV in comparison to the DMP condition (ps < .05). There were no significant differences between Tasks at Fz (ps > .05). When P3b latency was analysed using a two-way ANOVA, neither main effect was significant, but the Task × Midline electrode interaction was significant, F(4, 60) = 2.94, p < .05. Tukey HSD post hoc tests indicated that at Cz, P3b latency for the DMP condition (M = 435.9, S.E.M. = 22.83) was significantly longer in comparison to the SV condition (M = 414.0, S.E.M. = 20.15) (p < .05), but not significantly different to the DVP condition (M = 441.5, S.E.M. = 22.29). Again, analyses across hemispheres did not show any theoretically significant results. Relative to the SV task, there was a significant increase in RT for both dual task conditions indicating an overall dual task effect. Compared to the SM condition, there was a significant reduction in pattern stability for the DVP condition. However, there was no significant difference in pattern stability between the SM task and the DMP task, indicating that attention to the motor task prevented a loss of coordination stability under dual task conditions. This was also accompanied by a significant increase in RT relative to the DVP condition, representing the central cost associated with stabilising the coordination pattern. It could be argued that loss of stability occurred due to structural interference from discrete responses to the visual task however stability was measured pre and post common stimuli, which did not require an overt response. The only difference between the two dual task conditions was the attentional priority allocated to each task. The above prioritisation effects are in line with previous behavioural research investigating performance trade-offs under divided attention relative to attentional priority conditions using a probe RT [20]. However, due to the need to minimise fatigue and learning effects and maximise the number of low probability target stimuli for analysis, a divided attention control condition was not included in the current study. Although this prevents the dissociation of the relative effects of attention to the visual or motor task under dual-task conditions, the reductions in dual-task performance relative to single task performance when
attention is directed to either task indicates that attention was successfully manipulated and allows adequate assessment of the relative influence of attentional priority. The pattern observed in the behavioural data when the motor task was prioritised relative to when the visual task is prioritised is consistent with previous research in which performance trade-offs due to central cost (reduced stability and increased probe RT) have been observed as a function of priority [19]. Although it is argued that probe RT indexes the central cost or attentional load associated with stabilising coordinative patterns [10], it is likely that RT includes both central and response related resources and thus it may not be possible to completely dissociate these processes from behavioural measures alone. The P3b and P3a components are considered to index the allocation of central/perceptual and automatic attentional resources that are relatively independent of the resources associated with response preparation or execution (see [8,15]). In the present study P3a amplitude elicited by distracter visual stimuli was maximal at fronto-central midline electrodes, suggesting that the distracter stimulus elicited a P3a similar to that typically observed by novel stimuli [1,2]. There was an overall significant reduction in P3a amplitude under both dual task conditions relative to the single task condition, suggesting an overlap of a limited resource by the two tasks being performed [22,23] and a reduction in resources available for the automatic classification of distracter stimuli within the context of the visual task. However, there was also a significant reduction in P3a amplitude for the DMP relative to the DVP condition suggesting an additional reduction in automatic attentional resources available to evaluate distracter stimuli when attentional resources are allocated to the coordination task. These findings are not likely to be related to a reduction in response related resources as the distracter visual stimuli did not require an overt response. It has been suggested that the P3a component, when fronto-centrally maximal, reflects automatic attentional control mechanisms mediated by the frontal attentional network and may be related to working memory processes [13]. At central and parietal electrodes, prioritisation of the motor task resulted in a reduction in P3b amplitude relative to the single task condition. This is consistent with previous research finding a graded decrease in P3b amplitude as a function of attentional priority [18] and indicates a reduction in the cen-
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tral/perceptual resources available to perform the visual task. Considering that stability of coordination was maintained under this condition, P3b can be assumed to index the central cost associated with stabilisation of the coordination pattern [10]. When the visual task was prioritised, no reduction in P3b amplitude was found, despite a significant increase in RT relative to single task performance. This increase in RT, along with the decrease in coordination stability for this condition, may reflect an overall dual task effect due to the difficulty of the visual task. At the central electrode, prioritisation of the motor task also resulted in significant increase in P3b latency relative to the single visual task indicating an increase in stimulus evaluation time under these conditions. It has been suggested that the P3b component may index memory updating mechanisms subserved by temporal/parietal areas [13]. The present study was designed to investigate the electrophysiological correlates of the performance trade-off between coordination stability and central cost as a function of attentional priority [10]. The observed reduction in P3a amplitude under dual-task relative to the single task condition may indicate an overlap in resources related to the automatic attentional processing of stimuli by the two tasks being performed. The further reduction in P3a amplitude when the motor task was prioritised suggests that automatic attentional resources mediated by the frontal attentional network are also affected by the voluntary allocation of attention to the bimanual coordination task. The frontal attentional network (including areas such as the anterior cingulate gyrus (ACC), and lateral prefrontal cortex) has been shown to be involved in both complex motor control and the generation of P3a [4] and may be a possible locus for this effect. There was no loss of coordination stability under dual-task conditions in which the coordination task was prioritised and this was associated with an additional increase in RT, a decrease in parietal P3b amplitude, and an increase in central P3b latency to the visual target indexing the central cost of intentionally stabilising coordination under these conditions. Prioritisation of the visual task resulted in a significant reduction in both coordination stability and an increase in RT relative to single task conditions, though this was not accompanied by a significant reduction in P3b amplitude. The present study extends on previous research and demonstrates the utility of the P3b and P3a components for providing direct measures of the CNS activity associated with intentionally stabilising coordinative patterns. These indices allow insight into the types of resources or processes involved and are less likely to include the contribution of structural or response-related interference. Future research adopting this methodology may provide further insight into the relationship between coordination stability and central cost. Acknowledgment This work was supported by an ARC project grant (DPO451217) to the third and fourth authors.
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