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Reductions in neural activity underlie behavioral components of repetition priming

Abstract

Repetition priming is a nonconscious form of memory that is accompanied by reductions in neural activity when an experience is repeated. To date, however, there is no direct evidence that these neural reductions underlie the behavioral advantage afforded to repeated material. Here we demonstrate a causal linkage between neural and behavioral priming in humans. fMRI (functional magnetic resonance imaging) was used in combination with transcranial magnetic stimulation (TMS) to target and disrupt activity in the left frontal cortex during repeated classification of objects. Left-frontal TMS disrupted both the neural and behavioral markers of priming. Neural priming in early sensory regions was unaffected by left-frontal TMS—a finding that provides evidence for separable conceptual and perceptual components of priming.

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References

  1. 1

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

  2. 2

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

  3. 3

    Desimone, R. Neural mechanisms for visual memory and their role in attention. Proc. Natl. Acad. Sci. USA 93, 13494–13499 (1996).

  4. 4

    Miller, E.K., Li, L. & Desimone, R. A neural mechanism for working and recognition memory in inferior temporal cortex. Science 254, 1377–1379 (1991).

  5. 5

    Rainer, G. & Miller, E.K. Effects of visual experience on the representation of objects in the prefrontal cortex. Neuron 27, 179–189 (2000).

  6. 6

    Buckner, R.L. et al. Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron 20, 285–296 (1998).

  7. 7

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

  8. 8

    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).

  9. 9

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

  10. 10

    Maccotta, L. & Buckner, R.L. Evidence for neural effects of repetition that directly correlate with behavioral priming. J. Cogn. Neurosci. 16, 1625–1632 (2004).

  11. 11

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

  12. 12

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

  13. 13

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

  14. 14

    Henson, R.N. & Rugg, M.D. Neural response suppression, haemodynamic repetition effects, and behavioural priming. Neuropsychologia 41, 263–270 (2003).

  15. 15

    Schacter, D.L., Dobbins, I.G. & Schnyer, D.M. Specificity of priming: a cognitive neuroscience perspective. Nat. Rev. Neurosci. 5, 853–862 (2004).

  16. 16

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

  17. 17

    van Turennout, M., Ellmore, T. & Martin, A. Long-lasting cortical plasticity in the object naming system. Nat. Neurosci. 3, 1329–1334 (2000).

  18. 18

    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).

  19. 19

    Dobbins, I.G., Schnyer, D.M., Verfaellie, M. & Schacter, D.L. Cortical activity reductions during repetition priming can result from rapid response learning. Nature 428, 316–319 (2004).

  20. 20

    Friston, K.J., Frith, C.D., Passingham, R.E., Liddle, P.F. & Frackowiak, R.S. Motor practice and neurophysiological adaptation in the cerebellum: a positron tomography study. Proc. Biol. Sci. 248, 223–228 (1992).

  21. 21

    Grafton, S.T., Hazeltine, E. & Ivry, R. Functional mapping of sequence learning in normal humans. J. Cogn. Neurosci. 7, 497–510 (1995).

  22. 22

    Grafton, S.T., Hazeltine, E. & Ivry, R.B. Abstract and effector-specific representations of motor sequences identified with PET. J. Neurosci. 18, 9420–9428 (1998).

  23. 23

    Grafton, S.T. et al. Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J. Neurosci. 12, 2542–2548 (1992).

  24. 24

    Hazeltine, E., Grafton, S.T. & Ivry, R. Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. Brain 120, 123–140 (1997).

  25. 25

    van Mier, H., Tempel, L.W., Perlmutter, J.S., Raichle, M.E. & Petersen, S.E. Changes in brain activity during motor learning measured with PET: effects of hand of performance and practice. J. Neurophysiol. 80, 2177–2199 (1998).

  26. 26

    Ward, N.S., Brown, M.M., Thompson, A.J. & Frackowiak, R.S. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 126, 2476–2496 (2003).

  27. 27

    Karni, A. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158 (1995).

  28. 28

    Petersen, S.E., van Mier, H., Fiez, J.A. & Raichle, M.E. The effects of practice on the functional anatomy of task performance. Proc. Natl. Acad. Sci. USA 95, 853–860 (1998).

  29. 29

    Shadmehr, R. & Holcomb, H.H. Neural correlates of motor memory consolidation. Science 277, 821–825 (1997).

  30. 30

    Maccotta, L. & Buckner, R.L. Evidence for neural effects of repetition that directly correlate with behavioral priming. J. Cogn. Neurosci. 16, 1625–1632 (2004).

  31. 31

    Buckner, R.L., Koutstaal, W., Schacter, D.L. & Rosen, B.R. Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. Brain 123, 620–640 (2000).

  32. 32

    Dale, A.M. et al. Dynamic statistical parametric mapping: combining fMRI and MEG for high-resolution imaging of cortical activity. Neuron 26, 55–67 (2000).

  33. 33

    Donaldson, D.I., Petersen, S.E. & Buckner, R.L. Dissociating memory retrieval processes using fMRI: evidence that priming does not support recognition memory. Neuron 31, 1047–1059 (2001).

  34. 34

    Bergerbest, D., Ghahremani, D.G. & Gabrieli, J.D.E. Neural correlates of auditory repetition priming: Reduced fMRI activation in the auditory cortex. J. Cogn. Neurosci. 16, 966–977 (2004).

  35. 35

    Donaldson, D.I., Petersen, S.E. & Buckner, R.L. Dissociating memory retrieval processes using fMRI: Evidence that priming does not support recognition memory. Neuron 31, 1047–1059 (2001).

  36. 36

    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).

  37. 37

    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).

  38. 38

    Keane, M.M., Gabrieli, J.D., Fennema, A.C., Growdon, J.H. & Corkin, S. Evidence for a dissociation between perceptual and conceptual priming in Alzheimer's disease. Behav. Neurosci. 105, 326–342 (1991).

  39. 39

    Gabrieli, J.D.E., Fleischman, D.A., Keane, M.M.I., R.S. & Morell, F. Double dissociation between memory systems underlying explicit and implicit memory in the human brain. Psychol. Sci. 6, 76–82 (1995).

  40. 40

    Raczkowski, D., Kalat, J.W. & Nebes, R. Reliability and validity of some handedness questionnaire items. Neuropsychologia 12, 43–47 (1974).

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Acknowledgements

We thank R. Henson and A. Martin for their helpful comments on an earlier version of this manuscript, and R. Magge and T. Laroche for their technical assistance. This work was supported by a US National Institutes of Health grant (MH64667) to W.M.K. and the Dartmouth Brain Imaging Center. G.S.W. is a graduate fellow of the Natural Sciences and Engineering Research Council of Canada.

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Competing interests

The authors declare no competing financial interests.

Correspondence to Gagan S Wig.

Supplementary information

Supplementary Fig. 1

Post-TMS neural priming in the left posterior temporal cortex following left frontal and control-site TMS. (PDF 101 kb)

Supplementary Methods (PDF 135 kb)

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Figure 1: Experimental design.
Figure 2: TMS timing parameters.
Figure 3: Neural priming before TMS.
Figure 4: Neural priming after TMS.
Figure 5: Behavioral priming after left-frontal and control-site TMS.