Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

An electrophysiological signature of unconscious recognition memory

Abstract

Contradicting the common assumption that accurate recognition reflects explicit-memory processing, we provide evidence for recognition lacking two hallmark explicit-memory features: awareness of memory retrieval and facilitation by attentive encoding. Kaleidoscope images were encoded in conjunction with an attentional diversion and were subsequently recognized more accurately than those encoded without diversion. Confidence in recognition was superior following attentive encoding, although recognition was markedly accurate when people claimed to be unaware of memory retrieval. This 'implicit recognition' was associated with frontal-occipital negative brain potentials at 200–400 ms post-stimulus-onset, which were spatially and temporally distinct from positive brain potentials corresponding to explicit recollection and familiarity. This dissociation between behavioral and electrophysiological characteristics of 'implicit recognition' versus explicit recognition indicates that a neurocognitive mechanism with properties similar to those that produce implicit memory can be operative in standard recognition tests. People can accurately discriminate repeat stimuli from new stimuli without necessarily knowing it.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Schematic representation of experimental design.
Figure 2: Behavioral and ERP results.
Figure 3: Distinct temporal and topographic ERP patterns for accurate guess decisions compared with remember and know decisions.
Figure 4: Relationships between ERP correlates of recognition accompanied by remember, know, and guess decisions.

Similar content being viewed by others

References

  1. Claparéde, E. Recognition and 'me-ness'. in Organization and Pathology of Thought (ed. Rapaport, D.) 58–75 (Columbia University Press, New York, 1951).

    Google Scholar 

  2. Scoville, W.B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957).

    Article  CAS  Google Scholar 

  3. Schacter, D.L. Implicit memory: history and current status. J. Exp. Psychol. Learn. Mem. Cogn. 13, 501–518 (1987).

    Article  Google Scholar 

  4. Gabrieli, J.D. Cognitive neuroscience of human memory. Annu. Rev. Psychol. 49, 87–115 (1998).

    Article  CAS  Google Scholar 

  5. Squire, L.R. Memory systems of the brain: a brief history and current perspective. Neurobiol. Learn. Mem. 82, 171–177 (2004).

    Article  Google Scholar 

  6. Hamann, S.B. & Squire, L.R. Intact perceptual memory in the absence of conscious memory. Behav. Neurosci. 111, 850–854 (1997).

    Article  CAS  Google Scholar 

  7. Stark, C.E. & Squire, L.R. Recognition memory and familiarity judgments in severe amnesia: no evidence for a contribution of repetition priming. Behav. Neurosci. 114, 459–467 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Schacter, D.L., Wig, G.S. & Stevens, W.D. Reductions in cortical activity during priming. Curr. Opin. Neurobiol. 17, 171–176 (2007).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. 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).

    Article  CAS  Google Scholar 

  13. Rugg, M.D. et al. Dissociation of the neural correlates of implicit and explicit memory. Nature 392, 595–598 (1998).

    Article  CAS  Google Scholar 

  14. Schott, B., Richardson-Klavehn, A., Heinze, H.J. & Duzel, E. Perceptual priming versus explicit memory: dissociable neural correlates at encoding. J. Cogn. Neurosci. 14, 578–592 (2002).

    Article  Google Scholar 

  15. Schott, B.H. et al. Redefining implicit and explicit memory: the functional neuroanatomy of priming, remembering, and control of retrieval. Proc. Natl. Acad. Sci. USA 102, 1257–1262 (2005).

    Article  CAS  Google Scholar 

  16. Voss, J.L. & Paller, K.A. Fluent conceptual processing and explicit memory for faces are electrophysiologically distinct. J. Neurosci. 26, 926–933 (2006).

    Article  Google Scholar 

  17. Paller, K.A. & Gross, M. Brain potentials associated with perceptual priming vs explicit remembering during the repetition of visual word-form. Neuropsychologia 36, 559–571 (1998).

    Article  CAS  Google Scholar 

  18. Paller, K.A., Hutson, C.A., Miller, B.B. & Boehm, S.G. Neural manifestations of memory with and without awareness. Neuron 38, 507–516 (2003).

    Article  CAS  Google Scholar 

  19. Voss, J.L., Reber, P.J., Mesulam, M.M., Parrish, T.B. & Paller, K.A. Familiarity and conceptual priming engage distinct cortical networks. Cereb. Cortex 18, 1712–1719 (2008).

    Article  Google Scholar 

  20. Conroy, M.A., Hopkins, R.O. & Squire, L.R. On the contribution of perceptual fluency and priming to recognition memory. Cogn. Affect. Behav. Neurosci. 5, 14–20 (2005).

    Article  CAS  Google Scholar 

  21. Jacoby, L.L. & Whitehouse, K. An illusion of memory: false recognition influenced by unconscious perception. J. Exp. Psychol. Gen. 118, 126–135 (1989).

    Article  Google Scholar 

  22. Johnston, W.A., Hawley, K.J. & Elliott, J.M. Contribution of perceptual fluency to recognition judgments. J. Exp. Psychol. Learn. Mem. Cogn. 17, 210–223 (1991).

    Article  CAS  Google Scholar 

  23. Keane, M.M., Orlando, F. & Verfaellie, M. Increasing the salience of fluency cues reduces the recognition memory impairment in amnesia. Neuropsychologia 44, 834–839 (2006).

    Article  Google Scholar 

  24. Verfaellie, M. & Cermak, L.S. Perceptual fluency as a cue for recognition judgments in amnesia. Neuropsychology 13, 198–205 (1999).

    Article  CAS  Google Scholar 

  25. Voss, J.L., Baym, C.L. & Paller, K.A. Accurate forced-choice recognition without awareness of memory retrieval. Learn. Mem. 15, 454–459 (2008).

    Article  Google Scholar 

  26. Mulligan, N.W. The role of attention during encoding in implicit and explicit memory. J. Exp. Psychol. Learn. Mem. Cogn. 24, 27–47 (1998).

    Article  CAS  Google Scholar 

  27. Gardiner, J.M. & Java, R.I. Forgetting in recognition memory with and without recollective experience. Mem. Cognit. 19, 617–623 (1991).

    Article  CAS  Google Scholar 

  28. Mandler, G. Recognizing: the judgment of previous occurrence. Psychol. Rev. 87, 252–271 (1980).

    Article  Google Scholar 

  29. Yonelinas, A.P. The nature of recollection and familiarity: a review of 30 years of research. J. Mem. Lang. 46, 441–517 (2002).

    Article  Google Scholar 

  30. Yonelinas, A.P. Consciousness, control and confidence: the 3 Cs of recognition memory. J. Exp. Psychol. Gen. 130, 361–379 (2001).

    Article  CAS  Google Scholar 

  31. Mecklinger, A. Interfacing mind and brain: a neurocognitive model of recognition memory. Psychophysiology 37, 565–582 (2000).

    Article  CAS  Google Scholar 

  32. Paller, K.A., Voss, J.L. & Boehm, S.G. Validating neural correlates of familiarity. Trends Cogn. Sci. 11, 243–250 (2007).

    Article  Google Scholar 

  33. Rugg, M.D. & Curran, T. Event-related potentials and recognition memory. Trends Cogn. Sci. 11, 251–257 (2007).

    Article  Google Scholar 

  34. Voss, J.L. & Paller, K.A. Neural substrates of remembering: electroencephalographic studies. in Learning and Memory: a Comprehensive Reference (ed. Byrne, J.H.) 79–97 (Elsevier, Oxford, 2008).

    Chapter  Google Scholar 

  35. Vincent, J.L. et al. Coherent spontaneous activity identifies a hippocampal-parietal memory network. J. Neurophysiol. 96, 3517–3531 (2006).

    Article  Google Scholar 

  36. Curran, T. & Dien, J. Differentiating amodal familiarity from modality-specific memory processes: An ERP study. Psychophysiology 40, 979–988 (2003).

    Article  Google Scholar 

  37. Evans, K.M. & Federmeier, K.D. The memory that's right and the memory that's left: event-related potentials reveal hemispheric asymmetries in the encoding and retention of verbal information. Neuropsychologia 45, 1777–1790 (2007).

    Article  Google Scholar 

  38. Luck, S.J. & Hillyard, S.A. Electrophysiological correlates of feature analysis during visual search. Psychophysiology 31, 291–308 (1994).

    Article  CAS  Google Scholar 

  39. Misra, M. & Holcomb, P.J. Event-related potential indices of masked repetition priming. Psychophysiology 40, 115–130 (2003).

    Article  Google Scholar 

  40. Squire, L.R., Wixted, J.T. & Clark, R.E. Recognition memory and the medial temporal lobe: a new perspective. Nat. Rev. Neurosci. 8, 872–883 (2007).

    Article  CAS  Google Scholar 

  41. Wixted, J.T. Dual-process theory and signal-detection theory of recognition memory. Psychol. Rev. 114, 152–176 (2007).

    Article  Google Scholar 

  42. Wig, G.S., Grafton, S.T., Demos, K.E. & Kelley, W.M. Reductions in neural activity underlie behavioral components of repetition priming. Nat. Neurosci. 8, 1228–1233 (2005).

    Article  CAS  Google Scholar 

  43. Levy, D.A., Stark, C.E. & Squire, L.R. Intact conceptual priming in the absence of declarative memory. Psychol. Sci. 15, 680–686 (2004).

    Article  CAS  Google Scholar 

  44. Jacoby, L.L. & Dallas, M. On the relationship between autobiographical memory and perceptual learning. J. Exp. Psychol. Learn. Mem. Cogn. 110, 306–340 (1981).

    CAS  Google Scholar 

  45. Whittlesea, B.W. & Williams, L.D. The source of feelings of familiarity: the discrepancy-attribution hypothesis. J. Exp. Psychol. Learn. Mem. Cogn. 26, 547–565 (2000).

    Article  CAS  Google Scholar 

  46. Clayton, N.S., Bussey, T.J. & Dickinson, A. Can animals recall the past and plan for the future? Nat. Rev. Neurosci. 4, 685–691 (2003).

    Article  CAS  Google Scholar 

  47. Hampton, R.R. & Schwartz, B.L. Episodic memory in nonhumans: what, and where, is when? Curr. Opin. Neurobiol. 14, 192–197 (2004).

    Article  CAS  Google Scholar 

  48. Westerberg, C.E. et al. When memory does not fail: familiarity-based recognition in mild cognitive impairment and Alzheimer's disease. Neuropsychology 20, 193–205 (2006).

    Article  Google Scholar 

  49. Holdstock, J.S., Mayes, A.R., Gong, Q.Y., Roberts, N. & Kapur, N. Item recognition is less impaired than recall and associative recognition in a patient with selective hippocampal damage. Hippocampus 15, 203–215 (2005).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank S. Rearick for help with collecting pilot data and A. Gisbert and P. Reber for providing code used to generate stimuli. Financial support was provided by grants from the US National Institutes of Health (P30-AG13854) and National Science Foundation (0518800 and 0818912).

Author information

Authors and Affiliations

Authors

Contributions

Both authors designed the experiments, J.L.V. collected and analyzed the data, and both authors prepared the manuscript.

Corresponding author

Correspondence to Joel L Voss.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–3 (PDF 309 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voss, J., Paller, K. An electrophysiological signature of unconscious recognition memory. Nat Neurosci 12, 349–355 (2009). https://doi.org/10.1038/nn.2260

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2260

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing