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Perceiving patterns in random series: dynamic processing of sequence in prefrontal cortex

Abstract

We demonstrate that regions within human prefrontal cortex develop moment-to-moment models for patterns of events occurring in the sensory environment. Subjects viewed a random binary sequence of images, each presented singly and each requiring a different button press response. Patterns occurred by chance within the presented series of images. Using functional magnetic resonance imaging (fMRI), we identified activity evoked by viewing a stimulus that interrupted a pattern. Prefrontal activation was evoked by violations of both repeating and alternating patterns, and the amplitude of this activation increased with increasing pattern length. Violations of repeating patterns, but not of alternating patterns, activated the basal ganglia.

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Figure 1: A schematic representation of the experimental design and sequence analyses.
Figure 2: Behavioral results across stimulus sequences.
Figure 3: Brain regions associated with violations of stimulus pattern.
Figure 4: fMRI responses observed for violations of length 1–7 repeating patterns.
Figure 5: Dependence of HDR amplitude on stimulus pattern.

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References

  1. Canfield, R. L. & Haith, M. M. Young infants' visual expectations for symmetric and asymmetric stimulus sequences. Dev. Psychol. 27, 198–208 (1991).

    Article  Google Scholar 

  2. Cohen, A., Ivry, R. I. & Keele, S. W. Attention and structure in sequence learning. J. Exp. Psychol. Learn. Mem. Cogn. 16, 17–30 (1990).

    Article  Google Scholar 

  3. Curran, T. & Keele, S. W. Attentional and nonattentional forms of sequence learning. J. Exp. Psychol. Learn. Mem. Cogn. 19, 189–202 (1993).

    Article  Google Scholar 

  4. Willingham, D. B., Nissen, M. J. & Bullemer, P. On the development of procedural knowledge. J. Exp. Psychol. Learn. Mem. Cogn. 15, 1047–1060 (1989).

    Article  CAS  Google Scholar 

  5. Nissen, M. J. & Bullemer, P. Attentional requirements of learning: evidence from performance measures. Cognit. Psychol. 19, 1–32 (1987).

    Article  Google Scholar 

  6. Tversky, A. & Kahneman, D. Judgment under uncertainty: heuristics and biases. Science 185, 1124–1131 (1985).

    Article  Google Scholar 

  7. Hardoon, K. K., Baboushkin, H. R., Derevensky, J. L. & Gupta, R. Underlying cognitions in the selection of lottery tickets. J. Clin. Psychol. 57, 749–763 (2001).

    Article  CAS  Google Scholar 

  8. Squires, N., Squires, K. & Hillyard, S. A. Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. Electroencephalogr. Clin. Neurophysiol. 38 (1975).

  9. Courchesne, E., Hillyard, S. A. & Galambos, R. Stimulus novelty, task relevance, and the visual evoked potential in man. Electroencephalogr. Clin. Neurophysiol. 39, 131–143 (1975).

    Article  CAS  Google Scholar 

  10. Baudena, P., Halgren, E., Heit, G. & Clarke, J. M. Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. Electroencephalogr. Clin. Neurophysiol. 94, 251–264 (1995).

    Article  CAS  Google Scholar 

  11. McCarthy, G., Luby, M., Gore, J. & Goldman-Rakic, P. Infrequent events transiently activate human prefrontal and parietal cortex as measured by functional MRI. J. Neurophysiol. 77, 1630–1634 (1997).

    Article  CAS  Google Scholar 

  12. Kirino, E., Belger, A., Goldman-Rakic, P. & McCarthy, G. Prefrontal activation evoked by infrequent target and novel stimuli in a visual target detection task: an event-related functional magnetic resonance imaging study. J. Neurosci. 20, 6612–6618 (2000).

    Article  CAS  Google Scholar 

  13. Alain, C., Woods, D. L. & Knight, R. T. A distributed cortical network for auditory sensory memory in humans. Brain Res. 812, 23–37 (1998).

    Article  CAS  Google Scholar 

  14. Huettel, S. A. & Lockhead, G. R. Range effects of an irrelevant dimension on classification. Percept. Psychophys. 61, 1624–1646 (1999).

    Article  CAS  Google Scholar 

  15. Hyman, R. Stimulus information as a determinant of reaction time. J. Exp. Psychol. 45, 188–196 (1953).

    Article  CAS  Google Scholar 

  16. Bertelson, P. Sequential redundancy and speed in a serial two-choice responding task. Q. J. Exp. Psychol. 13, 90–102 (1961).

    Article  Google Scholar 

  17. Holland, M. K. & Lockhead, G. R. Sequential effects in absolute judgments of loudness. Percept. Psychophys. 3, 409–414 (1968).

    Article  Google Scholar 

  18. Schvaneveldt, R. W. & Chase, W. G. Sequential effects in choice reaction time. J. Exp. Psychol. 80, 1–8 (1969).

    Article  Google Scholar 

  19. Levy, R., Friedman, H. R., Davachi, L. & Goldman-Rakic, P. S. Differential activation of the caudate nucleus in primates performing spatial and nonspatial working memory tasks. J. Neurosci. 17, 3870–3882 (1997).

    Article  CAS  Google Scholar 

  20. Selemon, L. D. & Goldman-Rakic, P. S. Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J. Neurosci. 8, 4049–4068 (1988).

    Article  CAS  Google Scholar 

  21. Stevens, A. A., Skudlarski, P., Gatenby, J. C. & Gore, J. C. Event-related fMRI of auditory and visual oddball tasks. Magn. Reson. Imaging 18, 495–502 (2000).

    Article  CAS  Google Scholar 

  22. Clark, V. P., Fannon, S., Lai, S., Benson, R. & Bauer, L. Responses to rare visual target and distractor stimuli using event-related fMRI. J. Neurophysiol. 83, 3133–3139 (2000).

    Article  CAS  Google Scholar 

  23. Sohn, M., Ursu, S., Anderson, J. R., Stenger, V. A. & Carter, C. S. The role of prefrontal cortex and posterior parietal cortex in task switching. Proc. Natl. Acad. Sci. USA 97, 13448–1453 (2000).

    Article  CAS  Google Scholar 

  24. MacDonald, A. W., Cohen, J. D., Stenger, V. A. & Carter, C. S. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288, 1835–1838 (2000).

    Article  CAS  Google Scholar 

  25. Braver, T. S. et al. A parametric study of prefrontal cortex involvement in human working memory. NeuroImage 5, 49–62 (1997).

    Article  CAS  Google Scholar 

  26. Cohen, J. D. et al. Temporal dynamics of brain activation during a working memory task. Nature 386, 604–608 (1997).

    Article  CAS  Google Scholar 

  27. Harrington, D. L. et al. Specialized neural systems underlying representations of sequential movements. J. Cogn. Neurosci. 12, 56–77 (2000).

    Article  CAS  Google Scholar 

  28. Grafton, S. T., Fagg, A. H. & Arbib, M. A. Dorsal premotor cortex and conditional movement selection: a PET functional mapping study. J. Neurophysiol. 79, 1092–1097 (1998).

    Article  CAS  Google Scholar 

  29. Katayama, J. & Polich, J. Stimulus context determines P3a and P3b. Psychophysiology 35, 23–33 (1998).

    Article  CAS  Google Scholar 

  30. Comerchero, M. D. & Polich, J. P3a, perceptual distinctiveness, and stimulus modality. Cognit. Brain Res. 7, 41–48 (1998).

    Article  CAS  Google Scholar 

  31. Zatorre, R. J., Evans, A. C., Meyer, E. & Gjedde, A. Lateralization of phonetic and pitch discrimination in speech processing. Science 256, 846–849 (1992).

    Article  CAS  Google Scholar 

  32. Tervaniemi, M. et al. Lateralized automatic auditory processing of phonetic versus musical information: a PET study. Hum. Brain Mapp. 10, 74–79 (2000).

    Article  CAS  Google Scholar 

  33. Middleton, F. A. & Strick, P. L. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res. Rev. 31, 236–250 (2000).

    Article  CAS  Google Scholar 

  34. Gray, J. A. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 1165–1176 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  35. Hikosoka, O. et al. in The New Cognitive Neurosciences (ed. Gazzaniga, M. S.) 553–572 (MIT Press, Cambridge, Massachusetts, 1999).

    Google Scholar 

  36. Squires, K. C., Wickens, C., Squires, N. K. & Donchin, E. The effect of stimulus sequence on the waveform of the cortical event-related potential. Science 193, 1142–1145 (1976).

    Article  CAS  Google Scholar 

  37. Forman, S. D. et al. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33, 636–647 (1995).

    Article  CAS  Google Scholar 

  38. Xiong, J., Gao, J., Lancaster, J. L. & Fox, P. T. Clustered pixels analysis for functional MRI activation studies of the human brain. Hum. Brain Mapp. 3, 287–301 (1995).

    Article  Google Scholar 

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Acknowledgements

We thank C. Michelich, J. Voyvodic and J. Wu for assistance in data visualization and programming, and G. Lockhead, G. Mangun and D. Purves for comments on the manuscript. This research was supported by the US Department of Veterans' Affairs, by National Institute of Mental Health grants MH-05286 and MH-12541, and by National Institute of Neurological Disorders and Stroke grant NS-41328. G. M. is a Department of Veterans' Affairs Research Career Scientist.

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Correspondence to Gregory McCarthy.

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Huettel, S., Mack, P. & McCarthy, G. Perceiving patterns in random series: dynamic processing of sequence in prefrontal cortex. Nat Neurosci 5, 485–490 (2002). https://doi.org/10.1038/nn841

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