Cortical activity reductions during repetition priming can result from rapid response learning

Abstract

Recent observation of objects speeds up their subsequent identification and classification1,2. This common form of learning, known as repetition priming, can operate in the absence of explicit memory for earlier experiences3,4, and functional neuroimaging has shown that object classification improved in this way is accompanied by ‘neural priming’ (reduced neural activity) in prefrontal, fusiform and other cortical regions5,6,7,8,9,10. These observations have led to suggestions that cortical representations of items undergo ‘tuning’, whereby neurons encoding irrelevant information respond less as a given object is observed repeatedly10, thereby facilitating future availability of pertinent object knowledge. Here we provide experimental support for an alternative hypothesis, in which reduced cortical activity occurs because subjects rapidly learn their previous responses11. After a primed object classification (such as ‘bigger than a shoebox’), cue reversal (‘smaller than a shoebox’) greatly slowed performance and completely eliminated neural priming in fusiform cortex, which suggests that these cortical item representations were no more available for primed objects than they were for new objects. In contrast, prefrontal cortex activity tracked behavioural priming and predicted the degree to which cue reversal would slow down object classification—highlighting the role of the prefrontal cortex in executive control.

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Figure 1: Experiment design.
Figure 2: Behavioural reaction time data for scanned and finger-reversal experiments as a function of cue phase.
Figure 3: SPM results for novel versus high-primed responses across start, switch and return phases.

References

  1. 1

    Tulving, E. & Schacter, D. L. Priming and human memory systems. Science 247, 301–306 (1990)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Toth, J. P. & Reingold, E. M. in Implicit Cognition (ed. Underwood, G. D. M.) 41–84 (Oxford Univ. Press, London, 1996)

    Google Scholar 

  3. 3

    Squire, L. R. & McKee, R. Influence of prior events on cognitive judgments in amnesia. J. Exp. Psychol. 18, 106–115 (1992)

    CAS  Google Scholar 

  4. 4

    Schacter, D. L., Chiu, C. Y. P. & Ochsner, K. N. Implicit memory: A selective review. Annu. Rev. Neurosci. 16, 159–182 (1993)

    CAS  Article  Google Scholar 

  5. 5

    Raichle, M. E. et al. Practice-related changes in human brain functional anatomy during nonmotor learning. Cereb. Cortex 4, 8–26 (1994)

    CAS  Article  Google Scholar 

  6. 6

    Demb, J. B. et al. Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity. J. Neurosci. 15, 5870–5878 (1995)

    CAS  Article  Google Scholar 

  7. 7

    Buckner, R. L. et al. Functional anatomical studies of explicit and implicit memory retrieval tasks. J. Neurosci. 15, 12–29 (1995)

    CAS  Article  Google Scholar 

  8. 8

    Wagner, A. D., Desmond, J. E., Demb, J. B., Glover, G. H. & Gabrieli, J. D. E. Semantic repetition priming for verbal and pictorial knowledge: A functional MRI study of left inferior prefrontal cortex. J. Cogn. Neurosci. 9, 714–726 (1997)

    CAS  Article  Google Scholar 

  9. 9

    Schacter, D. L. & Buckner, R. L. Priming and the brain. Neuron 20, 185–195 (1998)

    CAS  Article  Google Scholar 

  10. 10

    Wiggs, C. L. & Martin, A. Properties and mechanisms of perceptual priming. Curr. Opin. Neurobiol. 8, 227–233 (1998)

    CAS  Article  Google Scholar 

  11. 11

    Logan, G. D. Repetition priming and automaticity: Common underlying mechanisms? Cognit. Psychol. 22, 1–35 (1990)

    Article  Google Scholar 

  12. 12

    Vriezen, E. R., Moscovitch, M. & Bellos, S. A. Priming effects in semantic classification tasks. J. Exp. Psychol. 21, 933–946 (1995)

    Google Scholar 

  13. 13

    Koutstaal, W. et al. Perceptual specificity in visual object priming: functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex. Neuropsychologia 39, 184–199 (2001)

    CAS  Article  Google Scholar 

  14. 14

    Thompson-Schill, S. L., D'Esposito, M. & Kan, I. P. Effects of repetition and competition on activity in left prefrontal cortex during word generation. Neuron 23, 513–522 (1999)

    CAS  Article  Google Scholar 

  15. 15

    Kane, M. J. & Engle, R. W. The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: an individual-differences perspective. Psychonom. Bull. Rev. 9, 637–671 (2002)

    Article  Google Scholar 

  16. 16

    Henson, R., Shallice, T. & Dolan, R. Neuroimaging evidence for dissociable forms of repetition priming. Science 287, 1269–1272 (2000)

    ADS  CAS  Article  Google Scholar 

  17. 17

    Gauthier, I. & Nelson, C. A. The development of face expertise. Curr. Opin. Neurobiol. 11, 219–224 (2001)

    CAS  Article  Google Scholar 

  18. 18

    Schacter, D. L. in Memory Systems of the Brain (eds Weinberger, N. M., McGaugh, J. L. & Lynch, G.) 351–379 (The Guilford Press, New York, 1985)

    Google Scholar 

  19. 19

    Hayman, C. G. & Tulving, E. Is priming in fragment completion based on a “traceless” memory system? J. Exp. Psychol. 15, 941–956 (1989)

    Google Scholar 

  20. 20

    Henson, R. N. Neuroimaging studies of priming. Prog. Neurobiol. 70, 53–81 (2003)

    CAS  Article  Google Scholar 

  21. 21

    Squire, L. R. et al. Activation of the hippocampus in normal humans: a functional anatomical study of memory. Proc. Natl Acad. Sci. USA 89, 1837–1841 (1992)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Schacter, D. L. et al. Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. Proc. Natl Acad. Sci. USA 93, 321–325 (1996)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Henson, R. N. et al. Electrophysiological and haemodynamic correlates of face perception, recognition and priming. Cereb. Cortex 13, 793–805 (2003)

    CAS  Article  Google Scholar 

  24. 24

    Simons, J. S., Koutstaal, W., Prince, S., Wagner, A. & Schacter, D. Neural mechanisms of visual object priming: Evidence for perceptual and semantic distinctions in fusiform cortex. Neuroimage 19, 613–626 (2003)

    Article  Google Scholar 

  25. 25

    Dale, A. M. Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 8, 109–114 (1999)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank L. Nicholls for help with data collection and analysis. This research was supported by grants from the NIMH (D.L.S. and D.M.S.), NINDS (M.V.) and the NIA (D.L.S.).

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Correspondence to Ian G. Dobbins.

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Dobbins, I., Schnyer, D., Verfaellie, M. et al. Cortical activity reductions during repetition priming can result from rapid response learning. Nature 428, 316–319 (2004). https://doi.org/10.1038/nature02400

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