Abstract
It is difficult to perform two tasks at the same time. Such performance limitations are exemplified by the psychological refractory period (PRP): when participants make distinct motor responses to two stimuli presented in rapid succession, the response to the second stimulus is increasingly slowed as the time interval between the two stimuli is decreased. This impairment is thought to reflect a central limitation in selecting the appropriate response to each stimulus, but not in perceptually encoding the stimuli. In the present study, it was sought to determine which brain regions are specifically involved in response selection under dual-task conditions by contrasting fMRI brain activity measured from a response selection manipulation that increased dual-task costs, with brain activity measured from an equally demanding manipulation that affected perceptual visibility. While a number of parieto-frontal areas involved in response selection were activated by both dual-task manipulations, the dorsal pre-motor cortex, and to a lesser extent the inferior frontal cortex, were specifically engaged by the response selection manipulation. These results suggest that the pre-motor cortex is an important neural locus of response selection limitation under dual-task situations.
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References
Allport, A. (1987). Selection for action: some behaviorial and neurophysiological considerations of attention and action. In: Heuer H., Sanders A. F. (eds.), Perspectives on perception and action. Erlbaum, Hillsdale, pp. 395–419.
Arnell K. M., & Duncan J. (2002). Separate and shared sources of dual-task cost in stimulus identification and response selection. Cognit Psychol 44:105–147.
Boussaoud D. (2001). Attention versus intention in the primate pre-motor cortex. NeuroImage, 14: S40–45.
Chun, M. M., & Potter, M. C. (1995). A two-stage model for multiple target detection in rapid serial visual presentation. J Exp Psychol: Hum Percept Perform, 21, 109–127.
Chun, M. M., & Potter, M. C. (2001). The attentional blink and task switching within and across modalities. In: Shapiro K. (Ed.), The limits of attention: temporal constraints in human information processing. Oxford University Press, NewYork, pp. 20–35.
De Jong, R. (1993). Multiple bottlenecks in overlapping task performance. J Exp Psychol: Hum Percept & Perform, 19, 965–980.
Decary, A., & Richer, F. (1995). Response selection deficits in frontal excisions. Neuropsychologia, 33, 1243–1253.
D’Esposito, M., Detre, J. A., Alsop, D. C., Shin, R. K., Atlas, S., & Grossman, M. (1995). The neural basis of the central executive system of working memory. Nature, 378, 279–281.
Dreher, J. C., & Grafman, J. (2003). Dissociating the roles of the rostral anterior cingulate and the lateral prefrontal cortices in performing two tasks simultaneously or successively. Cerebral Cortex, 13, 329–339.
Dum, R. P., & Strick, P. L. (2002). Motor areas in the frontal lobe of the primate, Physiol & Behav, 77, 677–682.
Duncan, J. (1980). The locus of interference in the perception of simultaneous stimuli. Psychological Review, 87, 272–300.
Duncan, J., & Owen, A. M. (2000). Common regions of the frontal lobe recruited by diverse cognitive demands. Trends Cognitive Sci, 23, 475–483.
Durston, S., Davidson, M.C., Thomas, K.M., Worden, M.S., Tottenham, N., Martinez, A., Watts, R., Ulug, A.M., & Casey, B.J. (2003). Parametric manipulation of conflict and response competition using rapid mixed-trial event-related fMRI. Neuroimage, 20, 2135–2141.
Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magnetic Resonance Medicine, 33, 636–647.
Gold, J. I., & Shadlen, M. N. (2001). Neural computations that underlie decisions about sensory stimuli. Trends Cognit Sci, 5, 10–16.
Hazeltine, E., Poldrack, R., & Gabrieli, J. D. E. (2000). Neural activation during response competition. J Cognit Neurosci, 12, 118–129.
Herath, P., Klingberg, T., Young, J., Amunts, K., & Roland, P. (2001). Neural correlates of dual task interference can be dissociated from those of divided attention: an fMRI study. Cerebral Cortex, 11, 796–805.
Hernandez, A., Zainos, A., & Romo, R. (2002). Temporal evolution of a decision-making process in medial pre-motor cortex. Neuron, 33, 959–972.
Ivry, R. B., Franz, E. A., Kingstone, A., & Johnston, J. C. (1998). The psychological refractory period effect following callosotomy: Uncoupling of lateralized response codes. J Exp Psychol: Hum Percept & Perform, 24, 463–480.
Jiang, Y. (2004) Resolving dual-task interference: an fMRI study. Neuroimage 22, 748–754.
Jiang, Y., & Kanwisher, N. (2003a). Common neural substrates for response selection across modalities and mapping paradigms. J Cognit Neurosci, 15, 1082–1094.
Jiang, Y., & Kanwisher, N. (2003b). Common neural mechanisms for response selection and perceptual processing. J Cognit Neurosci, 15, 1095–1110.
Jiang, Y., Saxe, R. & Kanwisher, N. (2004) Functional magnetic resonance imaging provides new constraints on theories of the psychological refractory period. Psychol Sci 15, 390–396.
Jolicoeur, P. (1998). Modulation of the attentional blink by on-line response selection: Evidence from speeded and unspeeded Task-sub-1 decisions. Memory & Cognition, 26, 1014–1032.
Jolicoeur, P. (1999). Dual-task interference and visual encoding. J Exp Psychol: Hum Percept & Perform, 25, 596–616.
Jolicoeur, P., Dell’ Acqua, R., & Crebolder, J. M. (2001). The attentional blink bottleneck. In K. Shapiro (Ed.), The limits of attention: temporal constraints in human information processing. OU Press, New York, pp. 82–99.
Kantowitz, B. H. (1974). Double stimulation. In B. H. Kantowitz (Ed.), Human information processing: Tutorials in performance and cognition. Erlbaum, Potomac, pp. 83–131.
Karlin, L., & Kestenbaum, R. (1968). Effects of number of alternatives on the psychological refractory period. Q J Exp Psychol, 20, 167–178.
Kimura, D. (1993). Neuromotor mechanisms in human communication. Oxford University Press, New York.
Kurata, K., Tsuji, T., Naraki, S., Seino, M., & Abe, Y. (2000). Activation of the dorsal pre-motor cortex and pre-supplementary motor area of humans during an auditory conditional motor task. J Neurophysiol, 84, 1667–1672.
Lee, K. M., Chang, K.-H., & Roh, J. K. (1999). Subregions within the supplementary motor area activated at different stages of movement preparation and execution. NeuroImage, 9, 117–123.
Luck, S. J. (1998). Sources of dual-task interference: evidence from human electrophysiology. Psychol Sci, 9, 223–227.
MacDonald, A. W., Cohen, J. D., Stenger, V. A., & Carter, C. S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288, 1835–1838.
Marois, R., Chun, M. M., & Gore, J. C. (2000). Neural correlates of the attentional blink. Neuron, 28, 299–308.
Marois, R., Chun, M. M., & Gore, J. C. (2004). A common parieto-frontal network is recruited under both low visibility and high perceptual interference. J Neurophysiol, 92, 2985–2992.
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annu Rev Neurosci, 24, 167–202.
Navon, D., & Miller, J. (2002). Queuing or Sharing? A Critical Evaluation of the Single-Bottleneck Notion. Cognit Psychol, 44, 193–251.
Osman, A., & Moore, C. M. (1993). The locus of dual-task interference: Psychological refractory effects on movement-related brain potentials. J Exp Psychol: Hum Percept & Perform, 19, 1292–1312.
Pashler, H. (1989). Dissociations and dependencies between speed and accuracy: Evidence for a two-component theory of divided attention in simple tasks. Cognit Psychol, 21, 469–514.
Pashler, H. (1994). Dual-task interference in simple tasks: Data and theory. Psychol Bull, 116, 220–244.
Pashler, H. E. (1998). The Psychology of Attention. MIT, Cambridge.
Pashler, H., & Johnston, J. C. (1989). Chronometric evidence for central postponement in temporally overlapping tasks. Q J Exp Psychol, 41A, 19–45.
Pashler, H., Luck, S. J., Hillyard, S. A., Mangun, G. R., O’Brien, S., & Gazzaniga, M. S. (1994). Sequential operation of disconnected cerebral hemispheres in split-brain patients. Neuroreport, 5, 2381–2384.
Passingham, R. E. (1993). The Frontal Lobes and Voluntary Action. Oxford UP, Oxford.
Picard, N., & Strick, P. L. (2001). Imaging the pre-motor areas. Curr Opinion Neurobiol, 11, 663–672.
Raymond, J. E., Shapiro, K. L., & Arnell, K. M. (1992). Temporary suppression of visual processing in an RSVP task: An attentional blink? J Exp Psychol: Hum Percept & Perform, 18, 849–860.
Rowe, J. B., Toni, I., Josephs, O., Frackowiak, R. S. J., & Passingham, R. E. (2000). The prefrontal cortex: response selection or maintenance within working memory? Science, 288, 1656–1660.
Rushworth, M. F., Nixon, P. D., Renowden, S., Wade, D. T., & Passingham, R. E. (1997). The left parietal cortex and motor attention. Neuropsychologia, 35, 1261–1273.
Rushworth, M. F., Paus, T., & Sipila, P. K. (2001a). Attention systems and the organization of the human parietal cortex. J Neurosci, 21, 5262–5271.
Rushworth, M. F. S., Krams, M., & Passingham, R. E. (2001b). The attentional role of the left parietal cortex: The distinct lateralization and localization of motor attention in the human brain. J Cognit Neurosci, 13, 698–710.
Rushworth, M. F. S., Hadland, K. A., Paus, T., & Sipila, P. K. (2002). Role of the Human Medial Frontal Cortex in Task Switching: A Combined fMRI and TMS Study. J Neurophysiol, 87, 2577–2592.
Ruthruff, E., Miller, J., & Lachmann, T. (1995). Does mental rotation require central mechanisms? J Exp Psychol: Hum Percept & Perform, 21, 552–570.
Ruthruff, E., & Pashler, H. (2001). Perceptual and central interference in dual-task performance. In K. Shapiro (Ed.), The limits of attention: temporal constraints in human information processing Oxford U Press, New York, pp. 100–123.
Schall, J. D. (2001). Neural basis of deciding, choosing and acting. Nat Rev Neurosci, 2, 33–42.
Schubert, T., & Szameitat, A. J. (2003). Functional neuroanatomy of interference in overlapping dual tasks: an fMRI study. Cognit Brain Res, 17, 733–746.
Schumacher, E. H., & D’Esposito, M. (2002). Neural implementation of response selection in humans as revealed by localized effects of stimulus-response compatibility on brain activation. Hum Brain Mapping, 17, 193–201.]
Schumacher, E. H., Elston, P.A., & D’Esposito, M. (2002). Neural evidence for representation-specific response selection. J Cognit Neurosci, 15, 1111–1121.
Shapiro, K., Hillstrom, A. P., & Husain, M. (2002). Control of Visuotemporal Attention by Inferior Parietal and Superior Temporal Cortex. Curr Biol, 12, 1320–1325.
Sternberg, S. (1969). The discovery of processing stages: Extensions of Donder’s method. Acta Psychologica, 30, 276–315.
Szameitat, A. J., Schubert, T., Muller, K., & von Cramon, D. Y. (2002). Localization of Executive Functions in Dual-Task Performance with fMRI. J Cognit Neurosci, 14, 1184–1199.
Talairach J, Tournoux P (1988). Co-planar stereotaxic atlas of the human brain. Thieme, New York.
Thompson-Schill, S. L., Swick, D., Farah, M. J., D’Esposito, M., Kan, I. P., & Knight, R. T. (1998). Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. Proc Natl Acad Sci USA, 95, 15855–15860.
Tombu, M., & Jolicoeur, P. (2003). A central capacity sharing model of dual-task performance. J Exp Psychol: Hum Percept and Perform, 29, 3–18.
Van Selst, M., & Jolicoeur, P. (1997). Decision and response in dual-task interference. Cognit Psychol, 33, 266–307.
Welford A. T. (1980). The single channel hypothesis. In A. T. Welford (Ed.), Reaction Time Academic Press, New York, pp. 215–252.
Welford, A. T. (1952). The “psychological refractory period” and the timing of high-speed performance: A review and theory. Br J Psychol, 43, 2–19.
Wise, S. P., & Murray, E. A. (2000). Arbitraty associations between antecedents and actions. Trends Neurosci, 23, 271–276.
Acknowledgements
The authors declare they have no financial conflict of interest regarding this study. We thank Jay Todd and Andy Snyder for expert technical assistance, and Gordon Logan, Jeff Schall, and Isabel Gauthier for helpful comments on earlier versions of the manuscript. This work was supported by NSF grant 0094992 and NIMH grant RO1MH70776 to R.M.
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Marois, R., Larson, J.M., Chun, M.M. et al. Response-specific sources of dual-task interference in human pre-motor cortex. Psychological Research 70, 436–447 (2006). https://doi.org/10.1007/s00426-005-0022-6
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DOI: https://doi.org/10.1007/s00426-005-0022-6