Antecedent acute cycling exercise affects attention control: an ERP study using attention network test

Yu-Kai Chang, Caterina Pesce, Yi-Te Chiang, Cheng-Yuh Kuo, Dong-Yang Fong, Yu-Kai Chang, Caterina Pesce, Yi-Te Chiang, Cheng-Yuh Kuo, Dong-Yang Fong

Abstract

The purpose of this study was to investigate the after-effects of an acute bout of moderate intensity aerobic cycling exercise on neuroelectric and behavioral indices of efficiency of three attentional networks: alerting, orienting, and executive (conflict) control. Thirty young, highly fit amateur basketball players performed a multifunctional attentional reaction time task, the attention network test (ANT), with a two-group randomized experimental design after an acute bout of moderate intensity spinning wheel exercise or without antecedent exercise. The ANT combined warning signals prior to targets, spatial cueing of potential target locations and target stimuli surrounded by congruent or incongruent flankers, which were provided to assess three attentional networks. Event-related brain potentials and task performance were measured during the ANT. Exercise resulted in a larger P3 amplitude in the alerting and executive control subtasks across frontal, central and parietal midline sites that was paralleled by an enhanced reaction speed only on trials with incongruent flankers of the executive control network. The P3 latency and response accuracy were not affected by exercise. These findings suggest that after spinning, more resources are allocated to task-relevant stimuli in tasks that rely on the alerting and executive control networks. However, the improvement in performance was observed in only the executively challenging conflict condition, suggesting that whether the brain resources that are rendered available immediately after acute exercise translate into better attention performance depends on the cognitive task complexity.

Keywords: alerting; executive function; interference control; orienting; spinning.

Figures

FIGURE 1
FIGURE 1
Illustration of the experimental procedure of the ANT. (A) An example of the sequence of events of the experimental procedure; (B) four cue conditions; and (C) response-stimulus (flanking) condition.
FIGURE 2
FIGURE 2
Reaction time (RT) as a function of the cue and flanking conditions (mean ± SE). ∗p < 0.05.
FIGURE 3
FIGURE 3
Reaction time (RT) as function of the cue and flanking conditions for the control and exercise groups separately for each network (mean ± SE). (A) Alerting network; (B) orienting network; and (C) executive control network. (D) RT differences between specific cue and flanking conditions that reflect the efficiency of the ANT networks for the control and exercise groups. ∗p < 0.05.
FIGURE 4
FIGURE 4
Event-related brain potential (ERP) data for the executive network task. (A) Grand averaged ERPs at Fz, Cz, and Pz for the exercise and control groups; (B) topographic maps of the voltage differences in the P3 component (300–500 ms) between the exercise and control groups.
FIGURE 5
FIGURE 5
Peak amplitude (mean and SE) of the P3 component of stimulus-locked ERPs for the alerting, orienting, and executive control networks in the ANT. Data are collapsed across midline electrodes (Fz, Cz, Pz) and presented separately for the exercise and the control group. ∗p < 0.05.

References

    1. American College of Sports Medicine. (2013). ACSM’s Guidelines for Exercise Testing and Prescription, 9th Edn. New York: Lippincott Williams and Wilkins.
    1. Bauman A., Bull F., Chey T., Craig C. L., Ainsworth B. E., Sallis J. F., et al. (2009). The international prevalence study on physical activity: results from 20 countries. Int. J. Behav. Nutr. Phys. Act. 6 21 10.1186/1479-5868-6-21
    1. Cahill L., Alkire M. T. (2003). Epinephrine enhancement of human memory consolidation: interaction with arousal at encoding. Neurobiol. Learn. Mem. 79 194–198 10.1016/S1074-7427(02)00036-9
    1. Callejas A., Lupiáñez J., Tudela P. (2004). The three attentional networks: on their independence and interactions. Brain Cogn. 54 225–227 10.1016/j.bandc.2004.02.012
    1. Cereatti L., Casella R., Manganelli M., Pesce C. (2009). Visual attention in adolescents: facilitating effects of sport expertise and acute physical exercise. Psychol. Sport Exerc. 10 136–145 10.1016/j.psychsport.2008.05.002
    1. Chang Y. K., Chi L., Etnier J. L., Wang C. C., Chu C. H., Zhou C. L. (2014). Effect of acute aerobic exercise on cognitive performance: role of cardiovascular fitness Psychol. Sport Exerc. 15 464–470 10.1016/j.physbeh.2011.06.005
    1. Chang Y. K., Labban J. D., Gapin J. I., Etnier J. L. (2012). The effects of acute exercise on cognitive performance: a meta-analysis. Brain Res. 1453 87–101 10.1016/j.brainres.2012.02.068
    1. Davranche K., Audiffren M. (2004). Facilitating effects of exercise on information processing. J. Sports Sci. 22 419–428 10.1080/02640410410001675289
    1. Davranche K., Hall B., McMorris T. (2009). Effect of acute exercise on cognitive control required during an Eriksen flanker task. J. Sport Exerc. Psychol. 31 628–639.
    1. Etnier J. L., Chang Y. K. (2009). The effect of physical activity on executive function: a brief commentary on definitions, measurement issues, and the current state of the literature. J. Sport Exerc. Psychol. 31 469–483.
    1. Fan J., Byrne J., Worden M. S., Guise K. G., McCandliss B. D., Fossella J., et al. (2007). The relation of brain oscillations to attentional networks. J. Neurosci. 27 6197–6206 10.1523/jneurosci.1833-07.2007.
    1. Fan J., Gu X., Guise K. G., Liu X., Fossella J., Wang H., et al. (2009). Testing the behavioral interaction and integration of attentional networks. Brain Cogn. 70 209–220 10.1016/j.bandc.2009.02.002
    1. Fan J., McCandliss B. D., Fossella J., Flombaum J. I., Posner M. I. (2005). The activation of attentional networks. Neuroimage 26 471–479 10.1016/j.neuroimage.2005.02.004
    1. Fan J., McCandliss B. D., Sommer T., Raz A., Posner M. I. (2002). Testing the efficiency and independence of attentional networks. J. Cogn. Neurosci. 14 340–347 10.1162/089892902317361886
    1. Galvao-Carmona A., González-Rosa J. J., Hidalgo-Muñoz A. R., Páramo D., Benítez M. L., Izquierdo G., et al. (2014). Disentangling the attention network test: behavioral, event related potentials, and neural source analyses. Front. Hum. Neurosci. 8:813 10.3389/fnhum.2014.00813
    1. Hillman C. H., Kamijo K., Scudder M. (2011). A review of chronic and acute physical activity participation on neuroelectric measures of brain health and cognition during childhood. Prev. Med. 52(Suppl. 1), S21–S28 10.1016/j.ypmed.2011.01.024
    1. Hillman C. H., Pontifex M., Themanson J. R. (2009). “Acute aerobic exercise effects on event-related brain potentials,” in Exercise and Cognitive Function, eds McMorris T., Tomporowski P. D., Audiffren M. (West Sussex: John Wiley and Sons; ), 161–178.
    1. Hillman C. H., Snook E. M., Jerome G. J. (2003). Acute cardiovascular exercise and executive control function. Int. J. Psychophysiol. 48 307–314 10.1016/S0167-8760(03)00080-1
    1. Huertas F., Zahonero J., Sanabria D., Lupianez J. (2011). Functioning of the attentional networks at rest vs. during acute bouts of aerobic exercise. J. Sport Exerc. Psychol. 33 649–665.
    1. Hung T. M., Tsai C. L., Chen F. T., Wang C. C., Chang Y. K. (2013). The immediate and sustained effects of acute exercise on planning aspect of executive function. Psychol. Sport Exerc. 14 728–736 10.1016/j.psychsport.2013.05.004
    1. Hüttermann S., Memmert D. (2014). Does the inverted-U function disappear in expert athletes? An analysis of the attentional behavior under physical exercise of athletes and non-athletes. Physiol. Behav. 131 87–92 10.1016/j.physbeh.2014.04.020
    1. Kamijo K., Hayashi Y., Sakai T., Yahiro T., Tanaka K., Nishihira Y. (2009). Acute effects of aerobic exercise on cognitive function in older adults. J. Gerontol. Ser. B Psychol. Sci. Soc. Sci. 64 356–363.
    1. Kamijo K., Nishihira Y., Hatta A., Kaneda T., Wasaka T., Kida T., et al. (2004). Differential influences of exercise intensity on information processing in the central nervous system. Eur. J. Appl. Physiol. 92 305–311 10.1007/s00421-004-1097-2
    1. Kamijo K., Nishihira Y., Higashiura T., Kuroiwa K. (2007). The interactive effect of exercise intensity and task difficulty on human cognitive processing. Int. J. Psychophysiol. 65 114–121 10.1016/j.ijpsycho.2007.04.001
    1. Kang J., Mangine G. T., Ratamess N. A., Faigenbaum A. D., Hoffman J. R. (2007). Influence of intensity fluctuation on exercise metabolism. Eur. J. Appl. Physiol. 100 253–260 10.1007/s00421-007-0424-9
    1. Lambourne K., Tomporowski P. (2010). The effect of exercise-induced arousal on cognitive task performance: a meta-regression analysis. Brain Res. 1341 12–24 10.1016/j.brainres.2010.03.091
    1. Llorens F., Sanabria D., Huertas F. (2014). The influence of acute intense exercise on exogenous spatial attention depends on physical fitness level. Exp. Psychol. 30 1–10.
    1. Lopez-Minarro P. A., Muyor Rodríguez J. M. (2010). Heart rate and overall ratings of perceived exertion during spinning cycle indoor session in novice adults. Sci. Sports 25 238–244 10.1016/j.scispo.2009.11.003
    1. Mahoney C. R., Hirsch E., Hasselquist L., Lesher L. L., Lieberman H. R. (2007). The effects of movement and physical exertion on soldier vigilance. Aviat. Space. Environ. Med. 78 B51–B57.
    1. McMorris T. (2008). Exercise and cognition: towards an inter-disciplinary model. Open. Sports Med. J. 2 60–68 10.2174/1874387000802010060
    1. Memmert D. (2009). Pay attention! A review of visual attentional expertise in sport. Int. Rev. Sport Exerc. Psychol. 2 119–138 10.1080/17509840802641372
    1. Neuhaus A. H., Urbanek C., Opgen-Rhein C., Hahn E., Ta T. M., Koehler S., et al. (2010). Event-related potentials associated with Attention Network Test. Int. J. Psychophysiol. 76 72–79 10.1016/j.ijpsycho.2010.02.005
    1. Pesce C. (2009). “An integrated approach to the effect of acute and chronic exercise on cognition: the linked role of individual and task constraints,” in Exercise and Cognitive Function, eds Mcmorris T., Tomporowski P. D., Audiffren M. (West Sussex: John Wiley and Sons; ), 213–226.
    1. Pesce C., Bosel R. (2001). Focusing of visuospatial attention: electrophysiological evidence from subjects with and without attentional expertise. J. Psychophysiol. 15 256–274 10.1027//0269-8803.15.4.256
    1. Pesce C., Cereatti L., Casella R., Baldari C., Capranica L. (2007a). Preservation of visual attention in older expert orienteers at rest and under physical effort. J. Sport Exerc. Psychol. 29 78–99.
    1. Pesce C., Tessitore A., Casella R., Pirritano M., Capranica L. (2007b). Focusing of visual attention at rest and during physical exercise in soccer players. J. Sports Sci. 25 1259–1270 10.1080/02640410601040085
    1. Pesce C., Cereatti L., Forte R., Crova C., Casella R. (2011). Acute and chronic exercise effects on attentional control in older road cyclists. Gerontology 57 121–128 10.1159/000314685
    1. Pontifex M. B., Hillman C. H. (2007). Neuroelectric and behavioral indices of interference control during acute cycling. Clin. Neurophysiol. 118 570–580 10.1016/j.clinph.2006.09.029
    1. Pontifex M. B., Hillman C. H. (2008). Neuroelectric measurement of cognition during aerobic exercise. Methods 45 271–278 10.1016/j.ymeth.2008.04.003
    1. Pontifex M. B., Saliba B. J., Raine L. B., Picchietti D. L., Hillman C. H. (2013). Exercise improves behavioral, neurocognitive, and scholastic performance in children with attention-deficit/hyperactivity disorder. J. Pediatr. 62 543–551 10.1016/j.jpeds.2012.08.036
    1. Posner M. I., Petersen S. E. (1990). The attention system of the human brain. Annu. Rev. Neurosci. 13 25–42 10.1146/annurev.ne.13.030190.000325
    1. Posner M. I., Rothbart M. K. (2007). Research on attention networks as a model for the integration of psychological science. Annu. Rev. Neurosci. 58 1–23.
    1. Sanabria D., Morales E., Luque A., Gálvez G., Huertas F., Lupiañez J. (2011). Effects of acute aerobic exercise on exogenous spatial attention. Psychol. Sport Exerc. 12 570–574 10.1016/j.psychsport.2011.04.002
    1. Smit A. S., Eling P. A., Hopman M. T., Coenen A. M. (2005). Mental and physical effort affect vigilance differently. Int. J. Psychophysiol. 57 211–217 10.1016/j.ijpsycho.2005.02.001
    1. Taddei F., Bultrini A., Spinelli D., Di Russo F. (2012). Neural correlates of attentional and executive processing in middle-age fencers. Med. Sci. Sports Exerc. 44 1057–1066 10.1249/MSS.0b013e31824529c2

Source: PubMed

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