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State-related and item-related neural correlates of successful memory encoding

Nature Neuroscience volume 5, pages 1339–1344 (2002)Cite this article

Abstract

Neuroimaging studies show that the efficacy of long-term memory encoding of a stimulus is indexed by transient neural activity elicited by that stimulus. Here, we show that successful memory encoding is also indexed by neural activity that is tonically maintained throughout a study task. Using functional magnetic resonance imaging (fMRI), transient and sustained neural activity were dissociated with a mixed event-related and blocked design. In a series of short task blocks, human subjects made semantic or phonological decisions about visually presented words. After statistically removing item-related activity, we found that the mean level of activity across a task block was correlated with the number of words subsequently remembered from that block. These correlations were found in inferior medial parietal and left prefrontal cortex for the semantic task, and in superior medial parietal cortex for the phonological task. Our findings suggest that state-related activity in these brain regions is involved in memory encoding.

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Figure 1: Methods.
Figure 2: State-related subsequent memory effects.
Figure 3: Time courses of state-related activity related to episodic encoding.
Figure 4: Item-related subsequent memory effects.

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References

  1. Rugg, M.D. in Handbook of Memory Disorders 2nd edn. (eds. Baddeley, B. et al.) (Wiley & Sons, Chichester, UK, in press).

  2. Buckner, R.L., Kelley, W.M. & Petersen, S.E. Frontal cortex contributes to human memory formation. Nat. Neurosci. 2, 311–314 (1999).

    Article  CAS  Google Scholar 

  3. Rosen, B.R. et al. Event-related functional MRI: past, present and future. Proc. Natl. Acad. Sci. USA 95, 773–780 (1998).

    Article  CAS  Google Scholar 

  4. Paller, K.A. & Wagner, A.D. Observing the transformation of experience into memory. Trends Cogn. Sci. 6, 93–102 (2002).

    Article  Google Scholar 

  5. Fernández, G. & Tendolkar, I. Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: human declarative memory formation at the system level. Brain Res. Bull. 55, 1–9 (2001).

    Article  Google Scholar 

  6. Fernández, G., Brewer, J.B., Zhao, Z., Glover, G.H. & Gabrieli, J.D.E. Level of sustained entorhinal activity at study correlates with subsequent cued-recall performance: a functional magnetic resonance imaging study with high acquisition rate. Hippocampus 9, 35–44 (1999).

    Article  Google Scholar 

  7. Chawla, D., Rees, G. & Friston, K.J. The physiological basis of attentional modulation in extrastriate visual areas. Nat. Neurosci. 2, 671–676 (1999).

    Article  CAS  Google Scholar 

  8. Donaldson, D.I., Petersen, S.E., Ollinger, J.M. & Buckner, R.L. Dissociating state and item components of recognition memory using fMRI. Neuroimage 13, 129–142 (2001).

    Article  CAS  Google Scholar 

  9. Otten, L.J. & Rugg, M.D. Task-dependency of the neural correlates of episodic encoding as measured by fMRI. Cereb. Cortex 11, 1150–1160 (2001).

    Article  CAS  Google Scholar 

  10. Snodgrass, J.G. & Corwin, J. Pragmatics of measuring recognition memory: applications to dementia and amnesia. J. Exp. Psychol. 117, 34–50 (1988).

    Article  CAS  Google Scholar 

  11. Wagner, A.D. et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281, 1188–1191 (1998).

    Article  CAS  Google Scholar 

  12. Brewer, J.B., Zhao, Z., Desmond, J.E., Glover, G.H. & Gabrieli, J.D.E. Making memories: brain activity that predicts how well visual experience will be remembered. Science 281, 1185–1187 (1998).

    Article  CAS  Google Scholar 

  13. Otten, L.J., Henson, R.N.A. & Rugg, M.D. Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. Brain 124, 399–412 (2001).

    Article  CAS  Google Scholar 

  14. Davachi, L., Maril, A. & Wagner, A.D. When keeping in mind supports later bringing to mind: neural markers of phonological rehearsal predict subsequent remembering. J. Cogn. Neurosci. 13, 1059–1070 (2001).

    Article  CAS  Google Scholar 

  15. Poldrack, R.A. et al. Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. Neuroimage 10, 15–35 (1999).

    Article  CAS  Google Scholar 

  16. Shallice, T. et al. Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature 368, 633–635 (1994).

    Article  CAS  Google Scholar 

  17. Bernstein, L.J., Beig, S., Siegenthaler, A.L. & Grady, C.L. The effect of encoding strategy on the neural correlates of memory for faces. Neuropsychologia 40, 86–98 (2002).

    Article  Google Scholar 

  18. Buckner, R.L., Wheeler, M.E. & Sheridan, M.A. Encoding processes during retrieval tasks. J. Cogn. Neurosci. 13, 406–415 (2001).

    Article  CAS  Google Scholar 

  19. Henson, R.N.A., Rugg, M.D., Shallice, T., Josephs, O. & Dolan, R.J. Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. J. Neurosci. 19, 3962–3972 (1999).

    Article  CAS  Google Scholar 

  20. Gusnard, D.A. & Raichle, M.E. Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci. 2, 685–694 (2001).

    Article  CAS  Google Scholar 

  21. Josephs, O. & Henson, R.N.A. Event-related functional magnetic resonance imaging: modelling, inference and optimisation. Phil. Trans. R. Soc. Lond. B Biol. Sci. 354, 1215–1228 (1999).

    Article  CAS  Google Scholar 

  22. Rugg, M.D., Otten, L.J. & Henson, R.N.A. The neural basis of episodic memory: evidence from functional neuroimaging. Phil. Trans. R. Soc. Lond. B Biol. Sci. 357, 1097–1110 (2002).

    Article  Google Scholar 

  23. Pashler, H., Johnston, J.C. & Ruthruff, E. Attention and performance. Annu. Rev. Psychol. 52, 629–651 (2001).

    Article  CAS  Google Scholar 

  24. Kucera, H. & Francis, W.N. Computational Analysis of Present-day American English (Brown Univ. Press, Providence, Rhode Island, 1967).

    Google Scholar 

  25. Friston, K.J. et al. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189–210 (1995).

    Article  Google Scholar 

  26. Ashburner, J. & Friston, K.J. Nonlinear spatial normalization using basis functions. Hum. Brain Mapp. 7, 254–266 (1999).

    Article  CAS  Google Scholar 

  27. Friston, K.J. et al. Event-related fMRI: characterising differential responses. Neuroimage 7, 30–40 (1998).

    Article  CAS  Google Scholar 

  28. Friston, K.J. Imaging cognitive anatomy. Trends Cogn. Sci. 1, 21–27 (1997).

    Article  Google Scholar 

  29. Holmes, A.P. & Friston, K.J. Generalisability, random effects and population inference. Neuroimage 7, 754 (1998).

    Article  Google Scholar 

  30. Otten, L.J. & Rugg, M.D. When more means less: neural activity related to unsuccessful memory encoding. Curr. Biol. 11, 1528–1530 (2001).

    Article  CAS  Google Scholar 

  31. Cocosco, C.A., Kollokian, V., Kwan, R.K.S. & Evans, A.C. BrainWeb: online interface to a 3D MRI simulated brain database. Neuroimage 5, S425 (1997).

    Google Scholar 

  32. Henson, R.N.A., Rugg, M.D. & Friston, K.J. The choice of basis functions in event-related fMRI. Neuroimage 13, 149 (2001).

    Article  Google Scholar 

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Acknowledgements

This work was supported by the Wellcome Trust and a cooperative award from the United Kingdom Medical Research Council. MRI scanning took place at the Wellcome Department of Imaging Neuroscience, Institute of Neurology, London, UK.

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Authors and Affiliations

  1. Institute of Cognitive Neuroscience, 17 Queen Square, London, WC1N 3AR, UK

    Leun J. Otten, Richard N. A. Henson & Michael D. Rugg

  2. Department of Psychology, University College London, 26 Bedford Way, London, WC1H 0AP, UK

    Leun J. Otten & Michael D. Rugg

  3. Wellcome Department of Imaging Neuroscience, 12 Queen Square, London, WC1N 3BG, UK

    Richard N. A. Henson

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  1. Leun J. Otten
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  3. Michael D. Rugg
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Correspondence to Leun J. Otten.

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Otten, L., Henson, R. & Rugg, M. State-related and item-related neural correlates of successful memory encoding. Nat Neurosci 5, 1339–1344 (2002). https://doi.org/10.1038/nn967

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