Motor Control, 2014, 18, 76-87 http://dx.doi.org/10.1123/mc.2012-0108 © 2014 Human Kinetics, Inc.
Dual Task Performance of the Stroop Color-Word Test and Stepping in Place Yoshifumi Ikeda, Hideyuki Okuzumi, and Mitsuru Kokubun This study investigated whether cognitive processing is influenced by stepping in place, particularly according to its frequency. Fourteen healthy young participants performed the Stroop test during stepping in place at various frequencies. Results showed the following: (a) performances on the Stroop test and at stepping in place at 1, 2, and 3 Hz were not so mutually influential, (b) performing the Stroop test degraded the timing of stepping in place at 4 Hz, (c) stepping at 0.5 Hz interfered with the cognitive processing involved with perceiving and naming colors but not with inhibitory control. These results imply that stepping in place is differentially controlled between walking at 1–4 Hz and at 0.5 Hz, the latter of which demands more attention. Keywords: attention, inhibitory control, executive function, gait, attractor
How cognition and movement affect one another has been of interest in recent years (Woollacott & Shumway-Cook, 2002). Their interaction is investigated typically in dual-task paradigms in which the two tasks can mutually compete. Specifically, many studies have examined how postural control or gait affects the performance of concurrent cognitive tasks (Boonyong, Siu, van Donkelaar, Chou, & Woollacott, 2012; Dault, Geurts, Mulder, & Duysens, 2001; Hollman, Kovash, Kubik, & Linbo, 2007; Lajoie, Teasdale, Bard, & Fleury, 1993; Olivier, Cuisinier, Vaugoyeau, Nougier, & Assaiante, 2010; Slobounov, Wu, & Hallett, 2006; Springer et al., 2006). Particularly, these studies examined the influence of postural control on different stances or support faces and the influence of cognitive tasks in different task loadings. However, it has rarely been investigated whether various gait properties influenced cognitive tasks. This study examined whether cognitive performance was affected by the gait property, defined herein as the frequency. Examining gait at various frequencies can be done by having a subject perform stepping in place at a fixed frequency imposed by the beeping of a metronome (Ikeda, Kamiyama, Okuzumi, Hirata, & Kokubun, 2011a; Okuzumi, Tanaka, & Haishi, 1997; Okuzumi, Tanaka, Haishi, & Sasaki, 1995). Ikeda et al. (2011a) examined the features of stepping in place at 0.5–4 Hz in terms of temporal and spatial variables and reported that the movement consistency was best at 2 Hz and at self-paced frequency. It deteriorated regardless of whether the step frequency became higher or lower. The authors are with the Dept. of Special Needs Education, Tokyo Gakugei University, Tokyo, Japan. 76
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Stroop Color-Word Test and Stepping in Place 77
One cognitive task used frequently in dual-task paradigms is the Stroop colorword test (Ikeda, Hirata, Okuzumi, & Kokubun, 2010; MacLeod, 1991; Stroop, 1935). In this test, participants are presented with color words displayed in an incongruent ink color (e.g., “red” written in blue). Then participants were instructed to name the ink color as quickly and accurately as possible. The performance in this “incongruent” condition is compared with the performance in a neutral condition, which requires naming the color of color patches. In general, latencies and the number of errors increased in the incongruent condition as compared with the neutral condition, which is designated as the Stroop interference (effect). To resolve Stroop interference, participants must inhibit the prepotent response of reading the color words and instead assign the nonprepotent response of naming the ink color. Therefore, the greater Stroop interference has been regarded as an index of lower inhibitory control (Friedman & Miyake, 2004; Ikeda, Okuzumi, Kokubun, & Haishi, 2011b). This study was designed to examine the interaction between the Stroop colorword test and stepping in place. Specifically, we investigate whether cognitive processing involved in the Stroop color-word test can be affected by concurrent stepping in place at various frequencies.
Methods Participants Fourteen adults (7 women, 7 men; mean age = 22.8 ± 2.4 years) were recruited for the study from a university in Tokyo, Japan. No participant had a prominent deficit in sensorimotor or cognitive skills or any hesitance at continuing the task. Informed consent was obtained from all participants before the assessment session.
Measures This study used a dual-task paradigm. Each participant was asked to perform the Stroop color–word test while stepping in place. Stepping in Place. Each participant, standing vertically on a flat floor with
a light emitting diode (LED) attached to the right ankle, was asked to step in place at five step-frequencies imposed by the beep of an electrical metronome (synchronized stepping). During synchronized stepping, participants kept time to the metronome by making the sole strike of the foot coincide with the metronome beat. Frequencies of the stimulus sounds were the following: 0.5 Hz (one sound for 2 s), 1 Hz (one sound for 1 s), 2 Hz (two sounds for 1 s), 3 Hz (three sounds for 1 s), and 4 Hz (four sounds for 1 s). Added to these synchronized stepping conditions, a self-paced stepping condition and a no-stepping condition (standing still) were also administered. During the experiments, temporal and spatial variables were measured. Specifically, vertical trajectories of the LED were recorded using a position sensor (C2399; Hamamatsu Photonics KK) from the right side of a participant and were subsequently converted to digital signals using an analog to digital (A/D) converter (NR-2000; Keyence Co.) at a sampling frequency of 100 Hz. All data were analyzed using spectral analyzer software (Wave Shot! 2000; Keyence Co.). The step time
78 Ikeda et al.
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was defined as the duration of each right step. The step frequency was calculated using the formulas presented below: step frequency = 2/step time. Stroop Color-Word Test. The Stroop color-word test was based on the procedure of Ikeda et al. (2011b) and controlled by SuperLab (Cedrus Corp., San Pedro, CA, USA). The test included two conditions: The neutral condition, in which participants named the colors of squares of four colors (red, blue, green, and yellow), and the incongruent condition, in which participants named the color of an incongruent stimulus. In the incongruent condition, the stimuli were four words (red, blue, yellow, and green) in Japanese characters, printed in a nonmatching color of the same four colors. For each task, each participant was asked to respond as quickly and accurately as possible to a series of eight stimuli displayed on a monitor positioned at a participant’s eye height, 100 cm in front of the participant. All stimuli were presented one at a time and randomly at the center of the white screen with a subsequent interstimulus interval during which a fixation cross was presented for 500 ms. All stimuli were replaced by the fixation cross when a participant’s voice key was input with a microphone connected to SuperLab. Thus, the stimulus presentation was not controlled to match with the metronome beat. The response time (RT) was recorded in milliseconds between the presentation of a stimulus and the onset of the participant’s vocal response. Two pretrials were administered before each condition.
Procedures Our experimental protocol was administered in accordance with the guidelines of the Declaration of Helsinki and was approved by the institutional review board. The experiments were administered to participants in a quiet room of a university. Each participant conducted the Stroop color-word test and the stepping in place simultaneously: the dual-task paradigm. For stepping in place, the order of performing six conditions was randomized for each participant. For each step frequency condition, two conditions of the Stroop color-word test were administered sequentially; the neutral condition preceded the incongruent condition to elicit the Stroop interference robustly. At the beginning of the testing, a participant was asked to step in place to the metronome beats several times. The Stroop color-word test started after a participant was judged to be performing stable synchronized stepping. The first three seconds of dual-tasking were excluded from analysis to avoid compromised measurements.
Results Means of Step Height Table 1 presents means and standard deviations of the step heights for each stepping condition. For both the neutral and the incongruent conditions, the step height decreased with higher step frequency. The step heights of self-paced stepping approximated 2 Hz. A 6 (step frequency: 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, 4 Hz, and self-paced) × 2 (cognitive task: neutral and incongruent) analysis of variance was conducted for the step heights. The analysis indicated significant main effect for the step frequency (F5, 65 = 12.41, p < .001, partial η2 = .49), but not for the cognitive
79
16.2
16.7
Neutral
Incongruent
M
9.6
9.3
SD
0.5 Hz
15.1
14.9
M 9.2
9.9
SD
1 Hz
11.5
11.8
M 5.4
5.1
SD
2 Hz
7.0
7.3
M 3.0
3.4
SD
3 Hz
Table 1 Means and Standard Deviations of Step Height (cm)
5.3
5.5
M
3.7
3.5
SD
4 Hz
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11.2
11.1
M
6.0
5.9
SD
Self-Paced
80 Ikeda et al.
task (F1, 13 = 0.01, ns, partial η2 = .001) or interaction between the step frequency and the cognitive task (F5, 65 = 0.33, ns, partial η2 = .02).
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Means of Step Frequency Table 2 presents means and standard deviations of the step frequencies for each stepping condition. For both the neutral and the incongruent conditions, the step frequencies of synchronized stepping coincided closely with stimulus frequencies, except for the 4 Hz condition. For the difference between step frequency and stimulus frequency, a 5 (step frequency: 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, and 4 Hz) × 2 (cognitive task: neutral and incongruent) analysis of variance was conducted. The analysis indicated significant main effect for the step frequency (F4, 52 = 12.13, p < .001, partial η2 = .48), but not for the cognitive task (F1, 13 = 1.83, ns, partial η2 = .12) or interaction between the step frequency and the cognitive task (F4, 52 = 0.55, ns, partial η2 = .04). Post hoc Bonferroni tests yielded significant between-step frequency comparisons between the 4 Hz condition and the other conditions (p < .05). Among the latter conditions, no further comparisons were significant. Moreover, the step frequencies of self-paced stepping approximated 2 Hz. For mean step frequency, a 6 (step frequency: 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, 4 Hz, and self-paced) × 2 (cognitive task: neutral and incongruent) analysis of variance was conducted. The analysis indicated significant main effect of the step frequency (F5, 2 65 = 450.23, p < .001, partial η = .97), but not for the cognitive task (F1, 13 = 2.18, 2 ns, partial η = .14) or interaction between the step frequency and the cognitive task (F5, 65 = 0.55, ns, partial η2 = .04). Post hoc Bonferroni tests yielded all significant between-step frequency comparisons, except for that between the 2 Hz condition and self-paced condition, for each cognitive task (p < .001).
Coefficient of Variation (CV) of Step Frequency The CV is defined as the ratio of the standard deviation to the mean. Figure 1 presents means and standard deviations of CV of the step frequency. Across all conditions, the CVs of the step frequencies were comparable between the two cognitive tasks. For both cognitive tasks, the CV of the step frequency was lowest at 2 Hz. It became higher whether the frequency was higher or lower. The coefficients of determination of the regression curves were very high when calculated for synchronized stepping (neutral, R2 = .948; incongruent, R2 = .977). The CVs of self-paced stepping were as low as those of 2 Hz conditions across cognitive task. A 6 (step frequency: 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, 4 Hz, and self-paced) × 2 (cognitive task: neutral and incongruent) analysis of variance was conducted for the CVs of step frequency. The analysis indicated significant main effect for the step frequency (F5, 65 = 4.77, p < .01, partial η2 = .27), but not for the cognitive task (F1, 13 = 0.62, ns, partial η2 = .02) or interaction between the step frequency and the cognitive task (F5, 65 = 1.98, p = .093, partial η2 = .13) although the interaction was marginally significant. Post hoc Bonferroni tests yielded significant betweenstep frequency comparisons between the 4 Hz condition and the 2 Hz condition (p < .05) and between the 4 Hz condition and the self-paced condition (p < .05). No further comparisons were significant.
81
SD
0.05
0.05
M
0.53
0.53
Neutral
Incongruent
0.5 Hz
1.07
1.06
M 0.27
0.27
SD
1 Hz
2.01
1.99
M 0.04
0.07
SD
2 Hz
2.90
2.86
M 0.17
0.15
SD
3 Hz
Table 2 Means and Standard Deviations of Step Frequency
3.61
3.60
M
0.31
0.36
SD
4 Hz
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2.01
1.98
M
0.16
0.18
SD
Self-Paced
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82 Ikeda et al.
Figure 1 — Means and standard deviations of CV of stepping frequency. Note: Upper error bars represent the standard deviation for the incongruence. Lower bars show the standard deviation for the neutral case.
Stroop Color-Word Test For the Stroop color-word test, no error was observed across neutral and incongruent conditions. Table 3 presents means and standard deviations of RT of the Stroop color–word test. Across all step frequencies, RT of the incongruent condition exceeded that of the neutral condition. In other words, Stroop interference was observed. For both Stroop conditions, RTs were comparable among all step frequencies, except for that between 0.5 Hz and the others. A seven (step frequency, 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, 4 Hz, self-paced, and no stepping) × two (cognitive task: neutral and incongruent) analysis of variance was conducted for RTs. The analysis yielded significant main effects for the step frequency (F6, 78 = 14.67, p < .001, partial η2 = .53) and the cognitive task (F1, 13 = 74.08, p < .001, partial η2 = .85), but not for interaction between the step frequency and the cognitive task (F6, 78 = 1.55, ns, partial η2 = .11). Post hoc Bonferroni tests showed significant differences between the 0.5 Hz and the others (p < .001), among which no further comparisons were significant.
Discussion This study was designed to examine the interaction between cognitive processing and a gait-like movement. Specifically, participants performed the Stroop colorword test during stepping in place at various step frequencies.
83
86
95
Incongruent 749
SD
691
Neutral
M
0.5 Hz
688
608
M 63
49
SD
1 Hz
677
570
M 67
92
SD
2 Hz
686
579
M 82
67
SD
3 Hz
691
579
M 66
51
SD
4 Hz
687
583
M
99
68
SD
Self-Paced
Table 3 Means and Standard Deviations of RT (ms) in the Stroop Color-Word Test
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698
575
M
53
51
SD
No Stepping
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84 Ikeda et al.
The results of stepping in place were mostly in line with those of a previous study of stepping in place without concurrent cognitive task (Ikeda et al., 2011a). With respect to temporal movement consistency, the results showed the highest temporal movement consistency around 2 Hz and that the movement consistency of self-paced stepping was as high as 2 Hz. In other words, the stepping around 2 Hz was optimized in terms of movement consistency. The phenomena related to self-optimization in gait have been reported in terms of spatial variability (Sekiya, Nagasaki, Ito, & Furuna, 1997), energy cost (Holt, Jeng, Ratcliffe, & Hamill, 1995), metabolic cost (Hunter & Smith, 2007), attentional demand (Kurosawa, 1994), veering (Uematsu et al., 2011), and the stability of head and pelvis acceleration (Latt, Menz, Fung, & Lord, 2008). According to the dynamical systems approach, self-optimization occurs to produce rhythmic movements on the attractor, a preferred state or sequence of states to which a system gravitates from arbitrary starting conditions and following arbitrary disturbances (Turvey, 1990). Thus, the results suggested that stepping in place around 2 Hz is on the attractor even when the concurrent cognitive task is performed. The differences were also apparent between stepping in place with and without concurrent cognitive tasks. With respect to coincidence between the step and stimulus, the results showed close coincidence between steps and the stimulus beeps although the frequency of stepping in place at 4 Hz condition was lower than the frequency of the stimulus. This might be interpreted as deterioration affected by the concurrent cognitive task because young adults can step in place precisely to the beep at 4 Hz with no concurrent task (Ikeda et al., 2011a). Moreover, the CVs of step frequencies in synchronized stepping conducted in this study were larger than stepping in place conducted in the study by Ikeda et al. (2011a). This can also be interpreted as deterioration affected by the concurrent cognitive task. The results of the Stroop color-word test indicated the following points. Whether stepping was conducted concurrently or not (no stepping) it did not affect the RTs of the Stroop color-word test, at least around 1–4 Hz. Together with the fact that the Stroop color-word test degraded the coincidence between steps and the stimulus beeps in stepping in place of 4 Hz condition, these results imply that stepping around 1–3 Hz needed less attentional resources that are shared with resolution of the Stroop color-word test. This might be plausible considering that stepping in place can be executed easily after motor planning including appropriate timing was set: actually, the analysis excluded the first few seconds, in which motor planning might be executed. The results also imply “posture second” or “cognition first” strategy rather than “posture first” strategy of gait (Bloem, Valkenburg, Slabbekoorn, & Willemsen, 2001) for the stepping around 1–4 Hz, given that the temporal movement consistency of stepping in place was degraded by the cognitive task. In contrast, stepping at 0.5 Hz affected the RT of the Stroop color-word test. This implies that stepping at 0.5 Hz was controlled by different mechanisms from stepping at 1–4 Hz and that it needed more attentional resources that share with resolving the Stroop color–word test. Ikeda et al. (2011a) also reported that stepping in place at 0.5 Hz might be controlled differently because it only demonstrated a developmental change. Because no other data are available regarding the difference between stepping at 0.5 Hz and the others, the underlying mechanisms cannot be explained fully in this study. For future studies, it might be important to consider
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Stroop Color-Word Test and Stepping in Place 85
the following points. First, stepping in place at low frequencies may be requiring more attentional resources because it may be less stable from a postural sense. A previous study showed that when walking at very low speeds, there is an activation of new muscles, presumably related to increased demands on postural stability (den Otter, Geurts, Mulder, & Duysens, 2004). Another study showed that longer single support time, which was probably the case in stepping in place at 0.5 Hz, demand greater postural attention (Lajoie et al., 1993). Second, stepping in place at low frequencies may be requiring more attentional resources because the stimulus beeps compete for attention as well. This will be particularly a factor for the slower (and faster) stepping in place where the participants must concentrate on the metronome beeps to meet the unnatural frequencies. Third and finally, rhythmic movements at lower frequencies resembled a sequence of discrete movements (Nagasaki, 1991), and it was revealed that discrete movements involve more cortical and subcortical activities (Schaal, Sternad, Osu, & Kawato, 2004), whereas rhythmic movement generation is associated primarily with pattern-generator circuits in the spinal cord and the brainstem (Marder, 2000). Stepping at 0.5 Hz affected the cognitive processing involved in the neutral condition, but not cognitive processing derived from the difference between the neutral and incongruent conditions, i.e., inhibitory control. This fact implies that attentional resources necessary for stepping at 0.5 Hz differ from those needed for inhibitory control. Although no statistical support was provided, it should be noted that the difference of RT between the neutral and incongruent conditions was smaller at the 0.5 Hz condition than at the other conditions. It would not be likely that stepping at 1–4 Hz required more attentional resources to resolve the Stroop interference. Instead, there appears to be a trade-off made between the Stroop colorword test and the stepping in place; relatively longer RTs for the neutral condition with stepping in place at 0.5 Hz could simply be because participants concentrated more on the stepping in place while they put more effort into the cognitive processing for the incongruent condition. One possible concern is that participants may have strategically or naturally tended to produce their responses for the Stroop color-word test at systematic times within the step cycle. This possibility cannot be excluded fully because this study did not record the step cycle and the vocal response by using the same software and analyze their synchronization. However, it should be noted that at least synchronization between the step cycle and the stimulus presentation can be excluded since the stimulus presentation time was varied for each trial. Another concern is related to whether participants made a normal stepping response, but moved very slowly, or they had extended dwell times with both feet on the floor and moved at a normal speed only when the next metronome beep was about to occur, for example in the 0.5 Hz condition. The following points should be considered. First, participants’ stepping in place were coordinated so as to keep the product of step frequency and step height almost constant, consistently with the study by Ikeda et al. (2011a). Second, before starting the dual-task phase, participants were judged by the experimenter that their sole strikes of the foot coincided closely with the metronome beat. There are some limitations in this study. The findings may be weakened by not including a condition where stepping in place is administered without the cognitive task. Moreover, the no-stepping condition required participants to stand still rather
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than to sit on a chair. Standing required more attentional demands on postural stability (Lajoie et al., 1993). Furthermore, stepping in place might not be referred to a gait-like task but a dynamic postural task at least for stepping in place at 0.5 Hz. In summary, results of this study demonstrated that in a dual task paradigm, stepping around 1–4 Hz deteriorated itself in terms of temporal movement consistency and coincidence with stimulus beep (for 4 Hz condition), but there was no deterioration of the performance of the Stroop color-word test, i.e., “posture second” strategy. Moreover, the results indicate that stepping at the 0.5 Hz degraded itself and the performance on the Stroop color-word test with respect to cognitive processing involved with perceiving and naming colors, but not with inhibitory control. Consequently, results of this study implied the difference in control mechanisms between stepping at the 0.5 Hz and the others. Nevertheless, the current data suggest no details related to this issue. Additional research is necessary to investigate the mechanisms using some analysis of step kinematics or brain imaging. Acknowledgments The authors thank all who participated in the study. This research was supported by a Japan Society for the Promotion of Science Research Fellowship for Young Scientists (to Y.I.).
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Ikeda, Y., Kamiyama, Y., Okuzumi, H., Hirata, S., & Kokubun, M. (2011a). Temporal and spatial parameters of stepping in place in children and adults. Perceptual and Motor Skills, 113, 331–338. PubMed doi:10.2466/06.11.23.25.26.PMS.113.4.331-338 Ikeda, Y., Okuzumi, H., Kokubun, M., & Haishi, K. (2011b). Age-related trends of interference control in school-age children and young adults in the Stroop color-word test. Psychological Reports, 108, 577–584. PubMed doi:10.2466/04.10.22.PR0.108.2.577-584 Kurosawa, K. (1994). Effects of various walking speeds on probe reaction time during treadmill walking. Perceptual and Motor Skills, 78, 768–770. PubMed doi:10.2466/ pms.1994.78.3.768 Lajoie, Y., Teasdale, N., Bard, C., & Fleury, M. (1993). Attentional demands for static and dynamic equilibrium. Experimental Brain Research, 97, 139–144. PubMed doi:10.1007/ BF00228824 Latt, M.D., Menz, H.B., Fung, V.S., & Lord, S.R. (2008). Walking speed, cadence and step length are selected to optimize the stability of head and pelvis accelerations. Experimental Brain Research, 184, 201–209. PubMed doi:10.1007/s00221-007-1094-x MacLeod, C.M. (1991). Half a century of research on the Stroop effect: an integrative review. Psychological Bulletin, 109, 163–203. PubMed doi:10.1037/0033-2909.109. 2.163 Marder, E. (2000). Motor pattern generation. Current Opinion in Neurobiology, 10, 691–698. PubMed doi:10.1016/S0959-4388(00)00157-4 Nagasaki, H. (1991). Asymmetrical trajectory formation in cyclic forearm movements in man. Experimental Brain Research, 87, 653–661. PubMed doi:10.1007/BF00227091 Okuzumi, H., Tanaka, A., & Haishi, K. (1997). Relationship between age and head movement during stepping in place by nonhandicapped children and persons with mental retardation. Perceptual and Motor Skills, 85, 375–381. PubMed doi:10.2466/ pms.1997.85.1.375 Okuzumi, H., Tanaka, A., Haishi, K., & Sasaki, T. (1995). Effect of tone on directional orientation during stepping in place with eyes closed. Perceptual and Motor Skills, 80, 719–722. PubMed doi:10.2466/pms.1995.80.3.719 Olivier, I., Cuisinier, R., Vaugoyeau, M., Nougier, V., & Assaiante, C. (2010). Age-related differences in cognitive and postural dual-task performance. Gait & Posture, 32, 494–499. PubMed doi:10.1016/j.gaitpost.2010.07.008 Schaal, S., Sternad, D., Osu, R., & Kawato, M. (2004). Rhythmic arm movement is not discrete. Nature Neuroscience, 7, 1136–1143. PubMed doi:10.1038/nn1322 Sekiya, N., Nagasaki, H., Ito, H., & Furuna, T. (1997). Optimal walking in terms of variability in step length. The Journal of Orthopaedic and Sports Physical Therapy, 26, 266–272. PubMed doi:10.2519/jospt.1997.26.5.266 Slobounov, S., Wu, T., & Hallett, M. (2006). Neural basis subserving the detection of postural instability: an fMRI study. Motor Control, 10, 69–89. PubMed Springer, S., Giladi, N., Peretz, C., Yogev, G., Simon, E.S., & Hausdorff, J.M. (2006). Dual-tasking effects on gait variability: the role of aging, falls, and executive function. Movement Disorders, 21, 950–957. PubMed doi:10.1002/mds.20848 Stroop, J.R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643–662. doi:10.1037/h0054651 Turvey, M.T. (1990). Coordination. The American Psychologist, 45, 938–953. PubMed doi:10.1037/0003-066X.45.8.938 Uematsu, A., Inoue, K., Hobara, H., Kobayashi, H., Iwamoto, Y., Hortobagyi, T., & Suzuki, S. (2011). Preferred step frequency minimizes veering during natural human walking. Neuroscience Letters, 505, 291–293. PubMed doi:10.1016/j.neulet.2011.10.057 Woollacott, M., & Shumway-Cook, A. (2002). Attention and the control of posture and gait: a review of an emerging area of research. Gait & Posture, 16, 1–14. PubMed doi:10.1016/S0966-6362(01)00156-4
Dual Task Performance of the Stroop Color-Word Test and Stepping in Place Yoshifumi Ikeda, Hideyuki Okuzumi, and Mitsuru Kokubun This study investigated whether cognitive processing is influenced by stepping in place, particularly according to its frequency. Fourteen healthy young participants performed the Stroop test during stepping in place at various frequencies. Results showed the following: (a) performances on the Stroop test and at stepping in place at 1, 2, and 3 Hz were not so mutually influential, (b) performing the Stroop test degraded the timing of stepping in place at 4 Hz, (c) stepping at 0.5 Hz interfered with the cognitive processing involved with perceiving and naming colors but not with inhibitory control. These results imply that stepping in place is differentially controlled between walking at 1–4 Hz and at 0.5 Hz, the latter of which demands more attention. Keywords: attention, inhibitory control, executive function, gait, attractor
How cognition and movement affect one another has been of interest in recent years (Woollacott & Shumway-Cook, 2002). Their interaction is investigated typically in dual-task paradigms in which the two tasks can mutually compete. Specifically, many studies have examined how postural control or gait affects the performance of concurrent cognitive tasks (Boonyong, Siu, van Donkelaar, Chou, & Woollacott, 2012; Dault, Geurts, Mulder, & Duysens, 2001; Hollman, Kovash, Kubik, & Linbo, 2007; Lajoie, Teasdale, Bard, & Fleury, 1993; Olivier, Cuisinier, Vaugoyeau, Nougier, & Assaiante, 2010; Slobounov, Wu, & Hallett, 2006; Springer et al., 2006). Particularly, these studies examined the influence of postural control on different stances or support faces and the influence of cognitive tasks in different task loadings. However, it has rarely been investigated whether various gait properties influenced cognitive tasks. This study examined whether cognitive performance was affected by the gait property, defined herein as the frequency. Examining gait at various frequencies can be done by having a subject perform stepping in place at a fixed frequency imposed by the beeping of a metronome (Ikeda, Kamiyama, Okuzumi, Hirata, & Kokubun, 2011a; Okuzumi, Tanaka, & Haishi, 1997; Okuzumi, Tanaka, Haishi, & Sasaki, 1995). Ikeda et al. (2011a) examined the features of stepping in place at 0.5–4 Hz in terms of temporal and spatial variables and reported that the movement consistency was best at 2 Hz and at self-paced frequency. It deteriorated regardless of whether the step frequency became higher or lower. The authors are with the Dept. of Special Needs Education, Tokyo Gakugei University, Tokyo, Japan. 76
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Stroop Color-Word Test and Stepping in Place 77
One cognitive task used frequently in dual-task paradigms is the Stroop colorword test (Ikeda, Hirata, Okuzumi, & Kokubun, 2010; MacLeod, 1991; Stroop, 1935). In this test, participants are presented with color words displayed in an incongruent ink color (e.g., “red” written in blue). Then participants were instructed to name the ink color as quickly and accurately as possible. The performance in this “incongruent” condition is compared with the performance in a neutral condition, which requires naming the color of color patches. In general, latencies and the number of errors increased in the incongruent condition as compared with the neutral condition, which is designated as the Stroop interference (effect). To resolve Stroop interference, participants must inhibit the prepotent response of reading the color words and instead assign the nonprepotent response of naming the ink color. Therefore, the greater Stroop interference has been regarded as an index of lower inhibitory control (Friedman & Miyake, 2004; Ikeda, Okuzumi, Kokubun, & Haishi, 2011b). This study was designed to examine the interaction between the Stroop colorword test and stepping in place. Specifically, we investigate whether cognitive processing involved in the Stroop color-word test can be affected by concurrent stepping in place at various frequencies.
Methods Participants Fourteen adults (7 women, 7 men; mean age = 22.8 ± 2.4 years) were recruited for the study from a university in Tokyo, Japan. No participant had a prominent deficit in sensorimotor or cognitive skills or any hesitance at continuing the task. Informed consent was obtained from all participants before the assessment session.
Measures This study used a dual-task paradigm. Each participant was asked to perform the Stroop color–word test while stepping in place. Stepping in Place. Each participant, standing vertically on a flat floor with
a light emitting diode (LED) attached to the right ankle, was asked to step in place at five step-frequencies imposed by the beep of an electrical metronome (synchronized stepping). During synchronized stepping, participants kept time to the metronome by making the sole strike of the foot coincide with the metronome beat. Frequencies of the stimulus sounds were the following: 0.5 Hz (one sound for 2 s), 1 Hz (one sound for 1 s), 2 Hz (two sounds for 1 s), 3 Hz (three sounds for 1 s), and 4 Hz (four sounds for 1 s). Added to these synchronized stepping conditions, a self-paced stepping condition and a no-stepping condition (standing still) were also administered. During the experiments, temporal and spatial variables were measured. Specifically, vertical trajectories of the LED were recorded using a position sensor (C2399; Hamamatsu Photonics KK) from the right side of a participant and were subsequently converted to digital signals using an analog to digital (A/D) converter (NR-2000; Keyence Co.) at a sampling frequency of 100 Hz. All data were analyzed using spectral analyzer software (Wave Shot! 2000; Keyence Co.). The step time
78 Ikeda et al.
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was defined as the duration of each right step. The step frequency was calculated using the formulas presented below: step frequency = 2/step time. Stroop Color-Word Test. The Stroop color-word test was based on the procedure of Ikeda et al. (2011b) and controlled by SuperLab (Cedrus Corp., San Pedro, CA, USA). The test included two conditions: The neutral condition, in which participants named the colors of squares of four colors (red, blue, green, and yellow), and the incongruent condition, in which participants named the color of an incongruent stimulus. In the incongruent condition, the stimuli were four words (red, blue, yellow, and green) in Japanese characters, printed in a nonmatching color of the same four colors. For each task, each participant was asked to respond as quickly and accurately as possible to a series of eight stimuli displayed on a monitor positioned at a participant’s eye height, 100 cm in front of the participant. All stimuli were presented one at a time and randomly at the center of the white screen with a subsequent interstimulus interval during which a fixation cross was presented for 500 ms. All stimuli were replaced by the fixation cross when a participant’s voice key was input with a microphone connected to SuperLab. Thus, the stimulus presentation was not controlled to match with the metronome beat. The response time (RT) was recorded in milliseconds between the presentation of a stimulus and the onset of the participant’s vocal response. Two pretrials were administered before each condition.
Procedures Our experimental protocol was administered in accordance with the guidelines of the Declaration of Helsinki and was approved by the institutional review board. The experiments were administered to participants in a quiet room of a university. Each participant conducted the Stroop color-word test and the stepping in place simultaneously: the dual-task paradigm. For stepping in place, the order of performing six conditions was randomized for each participant. For each step frequency condition, two conditions of the Stroop color-word test were administered sequentially; the neutral condition preceded the incongruent condition to elicit the Stroop interference robustly. At the beginning of the testing, a participant was asked to step in place to the metronome beats several times. The Stroop color-word test started after a participant was judged to be performing stable synchronized stepping. The first three seconds of dual-tasking were excluded from analysis to avoid compromised measurements.
Results Means of Step Height Table 1 presents means and standard deviations of the step heights for each stepping condition. For both the neutral and the incongruent conditions, the step height decreased with higher step frequency. The step heights of self-paced stepping approximated 2 Hz. A 6 (step frequency: 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, 4 Hz, and self-paced) × 2 (cognitive task: neutral and incongruent) analysis of variance was conducted for the step heights. The analysis indicated significant main effect for the step frequency (F5, 65 = 12.41, p < .001, partial η2 = .49), but not for the cognitive
79
16.2
16.7
Neutral
Incongruent
M
9.6
9.3
SD
0.5 Hz
15.1
14.9
M 9.2
9.9
SD
1 Hz
11.5
11.8
M 5.4
5.1
SD
2 Hz
7.0
7.3
M 3.0
3.4
SD
3 Hz
Table 1 Means and Standard Deviations of Step Height (cm)
5.3
5.5
M
3.7
3.5
SD
4 Hz
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11.2
11.1
M
6.0
5.9
SD
Self-Paced
80 Ikeda et al.
task (F1, 13 = 0.01, ns, partial η2 = .001) or interaction between the step frequency and the cognitive task (F5, 65 = 0.33, ns, partial η2 = .02).
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Means of Step Frequency Table 2 presents means and standard deviations of the step frequencies for each stepping condition. For both the neutral and the incongruent conditions, the step frequencies of synchronized stepping coincided closely with stimulus frequencies, except for the 4 Hz condition. For the difference between step frequency and stimulus frequency, a 5 (step frequency: 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, and 4 Hz) × 2 (cognitive task: neutral and incongruent) analysis of variance was conducted. The analysis indicated significant main effect for the step frequency (F4, 52 = 12.13, p < .001, partial η2 = .48), but not for the cognitive task (F1, 13 = 1.83, ns, partial η2 = .12) or interaction between the step frequency and the cognitive task (F4, 52 = 0.55, ns, partial η2 = .04). Post hoc Bonferroni tests yielded significant between-step frequency comparisons between the 4 Hz condition and the other conditions (p < .05). Among the latter conditions, no further comparisons were significant. Moreover, the step frequencies of self-paced stepping approximated 2 Hz. For mean step frequency, a 6 (step frequency: 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, 4 Hz, and self-paced) × 2 (cognitive task: neutral and incongruent) analysis of variance was conducted. The analysis indicated significant main effect of the step frequency (F5, 2 65 = 450.23, p < .001, partial η = .97), but not for the cognitive task (F1, 13 = 2.18, 2 ns, partial η = .14) or interaction between the step frequency and the cognitive task (F5, 65 = 0.55, ns, partial η2 = .04). Post hoc Bonferroni tests yielded all significant between-step frequency comparisons, except for that between the 2 Hz condition and self-paced condition, for each cognitive task (p < .001).
Coefficient of Variation (CV) of Step Frequency The CV is defined as the ratio of the standard deviation to the mean. Figure 1 presents means and standard deviations of CV of the step frequency. Across all conditions, the CVs of the step frequencies were comparable between the two cognitive tasks. For both cognitive tasks, the CV of the step frequency was lowest at 2 Hz. It became higher whether the frequency was higher or lower. The coefficients of determination of the regression curves were very high when calculated for synchronized stepping (neutral, R2 = .948; incongruent, R2 = .977). The CVs of self-paced stepping were as low as those of 2 Hz conditions across cognitive task. A 6 (step frequency: 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, 4 Hz, and self-paced) × 2 (cognitive task: neutral and incongruent) analysis of variance was conducted for the CVs of step frequency. The analysis indicated significant main effect for the step frequency (F5, 65 = 4.77, p < .01, partial η2 = .27), but not for the cognitive task (F1, 13 = 0.62, ns, partial η2 = .02) or interaction between the step frequency and the cognitive task (F5, 65 = 1.98, p = .093, partial η2 = .13) although the interaction was marginally significant. Post hoc Bonferroni tests yielded significant betweenstep frequency comparisons between the 4 Hz condition and the 2 Hz condition (p < .05) and between the 4 Hz condition and the self-paced condition (p < .05). No further comparisons were significant.
81
SD
0.05
0.05
M
0.53
0.53
Neutral
Incongruent
0.5 Hz
1.07
1.06
M 0.27
0.27
SD
1 Hz
2.01
1.99
M 0.04
0.07
SD
2 Hz
2.90
2.86
M 0.17
0.15
SD
3 Hz
Table 2 Means and Standard Deviations of Step Frequency
3.61
3.60
M
0.31
0.36
SD
4 Hz
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2.01
1.98
M
0.16
0.18
SD
Self-Paced
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82 Ikeda et al.
Figure 1 — Means and standard deviations of CV of stepping frequency. Note: Upper error bars represent the standard deviation for the incongruence. Lower bars show the standard deviation for the neutral case.
Stroop Color-Word Test For the Stroop color-word test, no error was observed across neutral and incongruent conditions. Table 3 presents means and standard deviations of RT of the Stroop color–word test. Across all step frequencies, RT of the incongruent condition exceeded that of the neutral condition. In other words, Stroop interference was observed. For both Stroop conditions, RTs were comparable among all step frequencies, except for that between 0.5 Hz and the others. A seven (step frequency, 0.5 Hz, 1 Hz, 2 Hz, 3 Hz, 4 Hz, self-paced, and no stepping) × two (cognitive task: neutral and incongruent) analysis of variance was conducted for RTs. The analysis yielded significant main effects for the step frequency (F6, 78 = 14.67, p < .001, partial η2 = .53) and the cognitive task (F1, 13 = 74.08, p < .001, partial η2 = .85), but not for interaction between the step frequency and the cognitive task (F6, 78 = 1.55, ns, partial η2 = .11). Post hoc Bonferroni tests showed significant differences between the 0.5 Hz and the others (p < .001), among which no further comparisons were significant.
Discussion This study was designed to examine the interaction between cognitive processing and a gait-like movement. Specifically, participants performed the Stroop colorword test during stepping in place at various step frequencies.
83
86
95
Incongruent 749
SD
691
Neutral
M
0.5 Hz
688
608
M 63
49
SD
1 Hz
677
570
M 67
92
SD
2 Hz
686
579
M 82
67
SD
3 Hz
691
579
M 66
51
SD
4 Hz
687
583
M
99
68
SD
Self-Paced
Table 3 Means and Standard Deviations of RT (ms) in the Stroop Color-Word Test
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698
575
M
53
51
SD
No Stepping
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84 Ikeda et al.
The results of stepping in place were mostly in line with those of a previous study of stepping in place without concurrent cognitive task (Ikeda et al., 2011a). With respect to temporal movement consistency, the results showed the highest temporal movement consistency around 2 Hz and that the movement consistency of self-paced stepping was as high as 2 Hz. In other words, the stepping around 2 Hz was optimized in terms of movement consistency. The phenomena related to self-optimization in gait have been reported in terms of spatial variability (Sekiya, Nagasaki, Ito, & Furuna, 1997), energy cost (Holt, Jeng, Ratcliffe, & Hamill, 1995), metabolic cost (Hunter & Smith, 2007), attentional demand (Kurosawa, 1994), veering (Uematsu et al., 2011), and the stability of head and pelvis acceleration (Latt, Menz, Fung, & Lord, 2008). According to the dynamical systems approach, self-optimization occurs to produce rhythmic movements on the attractor, a preferred state or sequence of states to which a system gravitates from arbitrary starting conditions and following arbitrary disturbances (Turvey, 1990). Thus, the results suggested that stepping in place around 2 Hz is on the attractor even when the concurrent cognitive task is performed. The differences were also apparent between stepping in place with and without concurrent cognitive tasks. With respect to coincidence between the step and stimulus, the results showed close coincidence between steps and the stimulus beeps although the frequency of stepping in place at 4 Hz condition was lower than the frequency of the stimulus. This might be interpreted as deterioration affected by the concurrent cognitive task because young adults can step in place precisely to the beep at 4 Hz with no concurrent task (Ikeda et al., 2011a). Moreover, the CVs of step frequencies in synchronized stepping conducted in this study were larger than stepping in place conducted in the study by Ikeda et al. (2011a). This can also be interpreted as deterioration affected by the concurrent cognitive task. The results of the Stroop color-word test indicated the following points. Whether stepping was conducted concurrently or not (no stepping) it did not affect the RTs of the Stroop color-word test, at least around 1–4 Hz. Together with the fact that the Stroop color-word test degraded the coincidence between steps and the stimulus beeps in stepping in place of 4 Hz condition, these results imply that stepping around 1–3 Hz needed less attentional resources that are shared with resolution of the Stroop color-word test. This might be plausible considering that stepping in place can be executed easily after motor planning including appropriate timing was set: actually, the analysis excluded the first few seconds, in which motor planning might be executed. The results also imply “posture second” or “cognition first” strategy rather than “posture first” strategy of gait (Bloem, Valkenburg, Slabbekoorn, & Willemsen, 2001) for the stepping around 1–4 Hz, given that the temporal movement consistency of stepping in place was degraded by the cognitive task. In contrast, stepping at 0.5 Hz affected the RT of the Stroop color-word test. This implies that stepping at 0.5 Hz was controlled by different mechanisms from stepping at 1–4 Hz and that it needed more attentional resources that share with resolving the Stroop color–word test. Ikeda et al. (2011a) also reported that stepping in place at 0.5 Hz might be controlled differently because it only demonstrated a developmental change. Because no other data are available regarding the difference between stepping at 0.5 Hz and the others, the underlying mechanisms cannot be explained fully in this study. For future studies, it might be important to consider
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Stroop Color-Word Test and Stepping in Place 85
the following points. First, stepping in place at low frequencies may be requiring more attentional resources because it may be less stable from a postural sense. A previous study showed that when walking at very low speeds, there is an activation of new muscles, presumably related to increased demands on postural stability (den Otter, Geurts, Mulder, & Duysens, 2004). Another study showed that longer single support time, which was probably the case in stepping in place at 0.5 Hz, demand greater postural attention (Lajoie et al., 1993). Second, stepping in place at low frequencies may be requiring more attentional resources because the stimulus beeps compete for attention as well. This will be particularly a factor for the slower (and faster) stepping in place where the participants must concentrate on the metronome beeps to meet the unnatural frequencies. Third and finally, rhythmic movements at lower frequencies resembled a sequence of discrete movements (Nagasaki, 1991), and it was revealed that discrete movements involve more cortical and subcortical activities (Schaal, Sternad, Osu, & Kawato, 2004), whereas rhythmic movement generation is associated primarily with pattern-generator circuits in the spinal cord and the brainstem (Marder, 2000). Stepping at 0.5 Hz affected the cognitive processing involved in the neutral condition, but not cognitive processing derived from the difference between the neutral and incongruent conditions, i.e., inhibitory control. This fact implies that attentional resources necessary for stepping at 0.5 Hz differ from those needed for inhibitory control. Although no statistical support was provided, it should be noted that the difference of RT between the neutral and incongruent conditions was smaller at the 0.5 Hz condition than at the other conditions. It would not be likely that stepping at 1–4 Hz required more attentional resources to resolve the Stroop interference. Instead, there appears to be a trade-off made between the Stroop colorword test and the stepping in place; relatively longer RTs for the neutral condition with stepping in place at 0.5 Hz could simply be because participants concentrated more on the stepping in place while they put more effort into the cognitive processing for the incongruent condition. One possible concern is that participants may have strategically or naturally tended to produce their responses for the Stroop color-word test at systematic times within the step cycle. This possibility cannot be excluded fully because this study did not record the step cycle and the vocal response by using the same software and analyze their synchronization. However, it should be noted that at least synchronization between the step cycle and the stimulus presentation can be excluded since the stimulus presentation time was varied for each trial. Another concern is related to whether participants made a normal stepping response, but moved very slowly, or they had extended dwell times with both feet on the floor and moved at a normal speed only when the next metronome beep was about to occur, for example in the 0.5 Hz condition. The following points should be considered. First, participants’ stepping in place were coordinated so as to keep the product of step frequency and step height almost constant, consistently with the study by Ikeda et al. (2011a). Second, before starting the dual-task phase, participants were judged by the experimenter that their sole strikes of the foot coincided closely with the metronome beat. There are some limitations in this study. The findings may be weakened by not including a condition where stepping in place is administered without the cognitive task. Moreover, the no-stepping condition required participants to stand still rather
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than to sit on a chair. Standing required more attentional demands on postural stability (Lajoie et al., 1993). Furthermore, stepping in place might not be referred to a gait-like task but a dynamic postural task at least for stepping in place at 0.5 Hz. In summary, results of this study demonstrated that in a dual task paradigm, stepping around 1–4 Hz deteriorated itself in terms of temporal movement consistency and coincidence with stimulus beep (for 4 Hz condition), but there was no deterioration of the performance of the Stroop color-word test, i.e., “posture second” strategy. Moreover, the results indicate that stepping at the 0.5 Hz degraded itself and the performance on the Stroop color-word test with respect to cognitive processing involved with perceiving and naming colors, but not with inhibitory control. Consequently, results of this study implied the difference in control mechanisms between stepping at the 0.5 Hz and the others. Nevertheless, the current data suggest no details related to this issue. Additional research is necessary to investigate the mechanisms using some analysis of step kinematics or brain imaging. Acknowledgments The authors thank all who participated in the study. This research was supported by a Japan Society for the Promotion of Science Research Fellowship for Young Scientists (to Y.I.).
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