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Decreased demands on cognitive control reveal the neural processing benefits of forgetting

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Abstract

Remembering often requires the selection of goal-relevant memories in the face of competition from irrelevant memories. Although there is a cost of selecting target memories over competing memories (increased forgetting of the competing memories), here we report neural evidence for the adaptive benefits of forgetting—namely, reduced demands on cognitive control during future acts of remembering. Functional magnetic resonance imaging during selective retrieval showed that repeated retrieval of target memories was accompanied by dynamic reductions in the engagement of functionally coupled cognitive control mechanisms that detect (anterior cingulate cortex) and resolve (dorsolateral and ventrolateral prefrontal cortex) mnemonic competition. Strikingly, regression analyses revealed that this prefrontal disengagement tracked the extent to which competing memories were forgotten; greater forgetting of competing memories was associated with a greater decline in demands on prefrontal cortex during target remembering. These findings indicate that, although forgetting can be frustrating, memory might be adaptive because forgetting confers neural processing benefits.

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Figure 1: Experimental protocol and behavioral results.
Figure 2: Dissociable neural correlates of retrieval success and repetition-related changes in the demands on cognitive control.
Figure 3: Neural predictors of mnemonic suppression.
Figure 4: MTL contributions to selective retrieval practice.

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  • 10 June 2007

    figure 3a y axis

Notes

  1. *NOTE: In the version of this article initially published online, the x-axis in Figure 3a was labeled incorrectly. The error has been corrected for all versions of the article.

References

  1. Levy, B.J. & Anderson, M.C. Inhibitory processes and the control of memory retrieval. Trends Cogn. Sci. 6, 299–305 (2002).

    Article  Google Scholar 

  2. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    Article  CAS  Google Scholar 

  3. Miller, E.K. & Cohen, J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    Article  CAS  Google Scholar 

  4. Bjork, R.A. Retrieval inhibition as an adaptive mechanism in human memory. in Varieties of Memory and Consciousness: Essays in Honor of Endel Tulving (eds. Roediger, H.L. & Craik, F.I.M.) 309–330 (Lawrence Erlbaum Associates, Inc., Hillsdale, NJ, 1989).

    Google Scholar 

  5. Anderson, M.C. Rethinking interference theory: executive control and the mechanisms of forgetting. J. Mem. Lang. 49, 414–445 (2003).

    Article  Google Scholar 

  6. Schacter, D.L. The seven sins of memory. Insights from psychology and cognitive neuroscience. Am. Psychol. 54, 182–203 (1999).

    Article  CAS  Google Scholar 

  7. Roediger, H.L. & McDermott, K.B. Tricks of memory. Curr. Dir. Psychol. Sci. 9, 123–127 (2000).

    Article  Google Scholar 

  8. Gates, A.I. Recitation as a factor in memorizing. Arch. Psychol. 6, 1–104 (1917).

    Google Scholar 

  9. Roediger, H.L. & Karpicke, J.D. Test-enhanced learning: taking memory tests improves long-term retention. Psychol. Sci. 17, 249–255 (2006).

    Article  Google Scholar 

  10. Anderson, M.C., Bjork, R.A. & Bjork, E.L. Remembering can cause forgetting: retrieval dynamics in long-term memory. J. Exp. Psychol. Learn. Mem. Cogn. 20, 1063–1087 (1994).

    Article  CAS  Google Scholar 

  11. Roediger, H.L. Inhibiting effects of recall. Mem. Cognit. 2, 261–269 (1974).

    Article  CAS  Google Scholar 

  12. Anderson, M.C. & Spellman, B.A. On the status of inhibitory mechanisms in cognition: memory retrieval as a model case. Psychol. Rev. 102, 68–100 (1995).

    Article  CAS  Google Scholar 

  13. Botvinick, M.M., Braver, T.S., Barch, D.M., Carter, C.S. & Cohen, J.D. Conflict monitoring and cognitive control. Psychol. Rev. 108, 624–652 (2001).

    Article  CAS  Google Scholar 

  14. Botvinick, M.M., Cohen, J.D. & Carter, C.S. Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn. Sci. 8, 539–546 (2004).

    Article  Google Scholar 

  15. MacDonald, A.W., III, 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 

  16. Shimamura, A. The role of the prefrontal cortex in dynamic filtering. Psychobiology 28, 207–218 (2000).

    Google Scholar 

  17. Anderson, M.C. et al. Neural systems underlying the suppression of unwanted memories. Science 303, 232–235 (2004).

    Article  CAS  Google Scholar 

  18. Badre, D. & Wagner, A.D. Selection, integration, and conflict monitoring; assessing the nature and generality of prefrontal cognitive control mechanisms. Neuron 41, 473–487 (2004).

    Article  CAS  Google Scholar 

  19. Aron, A.R., Fletcher, P.C., Bullmore, E.T., Sahakian, B.J. & Robbins, T.W. Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat. Neurosci. 6, 115–116 (2003).

    Article  CAS  Google Scholar 

  20. Aron, A.R., Robbins, T.W. & Poldrack, R.A. Inhibition and the right inferior frontal cortex. Trends Cogn. Sci. 8, 170–177 (2004).

    Article  Google Scholar 

  21. Cools, R., Clark, L., Owen, A.M. & Robbins, T.W. Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J. Neurosci. 22, 4563–4567 (2002).

    Article  CAS  Google Scholar 

  22. Chikazoe, J., Konishi, S., Asari, T., Jimura, K. & Miyashita, Y. Activation of right inferior frontal gyrus during response inhibition across response modalities. J. Cogn. Neurosci. 19, 69–80 (2007).

    Article  Google Scholar 

  23. Bunge, S.A., Dudukovic, N.M., Thomason, M.E., Vaidya, C.J. & Gabrieli, J.D. Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron 33, 301–311 (2002).

    Article  CAS  Google Scholar 

  24. Hazeltine, E., Poldrack, R. & Gabrieli, J.D. Neural activation during response competition. J. Cogn. Neurosci. 12, 118–129 (2000).

    Article  Google Scholar 

  25. Dobbins, I.G., Rice, H.J., Wagner, A.D. & Schacter, D.L. Memory orientation and success: separable neurocognitive components underlying episodic recognition. Neuropsychologia 41, 318–333 (2003).

    Article  Google Scholar 

  26. Kahn, I., Davachi, L. & Wagner, A.D. Functional-neuroanatomic correlates of recollection: implications for models of recognition memory. J. Neurosci. 24, 4172–4180 (2004).

    Article  CAS  Google Scholar 

  27. Buckner, R.L. & Wheeler, M.E. The cognitive neuroscience of remembering. Nat. Rev. Neurosci. 2, 624–634 (2001).

    Article  CAS  Google Scholar 

  28. Rugg, M.D. & Wilding, E.L. Retrieval processing and episodic memory. Trends Cogn. Sci. 4, 108–115 (2000).

    Article  CAS  Google Scholar 

  29. Henson, R.N., Rugg, M.D., Shallice, T. & Dolan, R.J. Confidence in recognition memory for words: dissociating right prefrontal roles in episodic retrieval. J. Cogn. Neurosci. 12, 913–923 (2000).

    Article  CAS  Google Scholar 

  30. McDermott, K.B., Jones, T.C., Petersen, S.E., Lageman, S.K. & Roediger, H.L., III Retrieval success is accompanied by enhanced activation in anterior prefrontal cortex during recognition memory: an event-related fMRI study. J. Cogn. Neurosci. 12, 965–976 (2000).

    Article  CAS  Google Scholar 

  31. Anderson, M.C., Bjork, E.L. & Bjork, R.A. Retrieval-induced forgetting: evidence for a recall-specific mechanism. Psychon. Bull. Rev. 7, 522–530 (2000).

    Article  CAS  Google Scholar 

  32. Thompson-Schill, S.L. & Botvinick, M.M. Resolving conflict: a response to Martin and Cheng (2006). Psychon. Bull. Rev. 13, 402–8–discussion 409–11 (2006).

    Article  Google Scholar 

  33. Kerns, J.G. et al. Anterior cingulate conflict monitoring and adjustments in control. Science 303, 1023–1026 (2004).

    Article  CAS  Google Scholar 

  34. Bunge, S.A., Burrows, B. & Wagner, A.D. Prefrontal and hippocampal contributions to visual associative recognition: interactions between cognitive control and episodic retrieval. Brain Cogn. 56, 141–152 (2004).

    Article  CAS  Google Scholar 

  35. Curtis, C.E. & D'Esposito, M. Persistent activity in the prefrontal cortex during working memory. Trends Cogn. Sci. 7, 415–423 (2003).

    Article  Google Scholar 

  36. Egner, T. & Hirsch, J. Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information. Nat. Neurosci. 8, 1784–1790 (2005).

    Article  CAS  Google Scholar 

  37. Weissman, D.H., Warner, L.M. & Woldorff, M.G. The neural mechanisms for minimizing cross-modal distraction. J. Neurosci. 24, 10941–10949 (2004).

    Article  CAS  Google Scholar 

  38. Cohen, N.J. & : Eichenbaum, H. Memory, Amnesia and the Hippocampal System (MIT Press, Cambridge, MA, 1993).

    Google Scholar 

  39. Rugg, M.D. & Yonelinas, A.P. Human recognition memory: a cognitive neuroscience perspective. Trends Cogn. Sci. 7, 313–319 (2003).

    Article  Google Scholar 

  40. Squire, L.R., Stark, C.E. & Clark, R.E. The medial temporal lobe. Annu. Rev. Neurosci. 27, 279–306 (2004).

    Article  CAS  Google Scholar 

  41. Kirwan, C.B. & Stark, C.E. Medial temporal lobe activation during encoding and retrieval of novel face-name pairs. Hippocampus 14, 919–930 (2004).

    Article  Google Scholar 

  42. Yonelinas, A.P., Otten, L.J., Shaw, K.N. & Rugg, M.D. Separating the brain regions involved in recollection and familiarity in recognition memory. J. Neurosci. 25, 3002–3008 (2005).

    Article  CAS  Google Scholar 

  43. Giovanello, K.S., Schnyer, D.M. & Verfaellie, M. A critical role for the anterior hippocampus in relational memory: evidence from an fMRI study comparing associative and item recognition. Hippocampus 14, 5–8 (2004).

    Article  Google Scholar 

  44. van Veen, V. & Carter, C.S. Separating semantic conflict and response conflict in the Stroop task: a functional MRI study. Neuroimage 27, 497–504 (2005).

    Article  Google Scholar 

  45. Brown, J.W. & Braver, T.S. Learned predictions of error likelihood in the anterior cingulate cortex. Science 307, 1118–1121 (2005).

    Article  CAS  Google Scholar 

  46. Raye, C.L., Johnson, M.K., Mitchell, K.J., Reeder, J.A. & Greene, E.J. Neuroimaging a single thought: dorsolateral PFC activity associated with refreshing just-activated information. Neuroimage 15, 447–453 (2002).

    Article  Google Scholar 

  47. Fletcher, P.C. & Henson, R.N. Frontal lobes and human memory: insights from functional neuroimaging. Brain 124, 849–881 (2001).

    Article  CAS  Google Scholar 

  48. Mensink, G. & Raaijmakers, J.G. A model for interference and forgetting. Psychol. Rev. 95, 434–455 (1988).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  50. Glover, G.H. & Law, C.S. Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn. Reson. Med. 46, 515–522 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

Supported by the National Institute of Mental Health (1R01MH080309–01), National Science Foundation (BCS–0401641), McKnight Endowment Fund for Neuroscience and Alfred P. Sloan Foundation.

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Correspondence to Brice A Kuhl.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Dissociations and overlap between effects of retrieval success and retrieval repetition. (PDF 275 kb)

Supplementary Table 1

Frontoparietal regions more active during first successful retrieval than third successful retrieval during retrieval practice. (PDF 50 kb)

Supplementary Table 2

Regions in which repetition-related changes in activation are predictive of long-term competitor forgetting. (PDF 47 kb)

Supplementary Methods (PDF 73 kb)

Supplementary Results (PDF 153 kb)

Supplementary Discussion (PDF 46 kb)

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Kuhl, B., Dudukovic, N., Kahn, I. et al. Decreased demands on cognitive control reveal the neural processing benefits of forgetting. Nat Neurosci 10, 908–914 (2007). https://doi.org/10.1038/nn1918

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