Emotional learning selectively and retroactively strengthens memories for related events

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Abstract

Neurobiological models of long-term memory propose a mechanism by which initially weak memories are strengthened through subsequent activation that engages common neural pathways minutes to hours later1. This synaptic tag-and-capture model has been hypothesized to explain how inconsequential information is selectively consolidated following salient experiences. Behavioural evidence for tag-and-capture is provided by rodent studies in which weak early memories are strengthened by future behavioural training2,3. Whether a process of behavioural tagging occurs in humans to transform weak episodic memories into stable long-term memories is unknown. Here we show, in humans, that information is selectively consolidated if conceptually related information, putatively represented in a common neural substrate, is made salient through an emotional learning experience. Memory for neutral objects was selectively enhanced if other objects from the same category were paired with shock. Retroactive enhancements as a result of emotional learning were observed following a period of consolidation, but were not observed in an immediate memory test or for items strongly encoded before fear conditioning. These findings provide new evidence for a generalized retroactive memory enhancement, whereby inconsequential information can be retroactively credited as relevant, and therefore selectively remembered, if conceptually related information acquires salience in the future.

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Figure 1: Incidental encoding paradigm and example stimuli.
Figure 2: Recognition memory performance.
Figure 3: Recognition memory difference scores.

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Acknowledgements

We thank G. L. Murphy for comments on the manuscript, and S. Lackovic and J. Reitzes for assistance with data collection. This study was supported by NIH RO1 MH097085, R01 MH047692, F31 DA036361, and NIMH Training Award in Systems and Integrative Neuroscience T32 MH019524.

Author information

J.E.D. designed and conducted the study. J.E.D. and V.P.M. analysed the data. J.E.D., V.P.M., L.D. and E.A.P. interpreted the results and wrote the manuscript.

Correspondence to Lila Davachi or Elizabeth A. Phelps.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Skin conductance responses.

Mean square-root-normalized skin conductive responses for the CS+ and CS for each group. Results provide confirmation that the fear-conditioning manipulation was effective at generating higher arousal in CS+ than CS trials. Error bars are s.e.m. P < 0.01, two-tailed t-tests.

Extended Data Figure 2 Individual data points overlaid on group means.

Note that some data points overlap for subjects with the same memory score.

Extended Data Figure 3 Recognition memory performance in the 24-h retrieval, strong-encoding group.

Memory at 24-h retrieval for the strong-encoding group showed no difference in recognition memory between the CS+ and CS items encoded before fear conditioning. Memory enhancements for stimuli encoded during fear conditioning were greater for CS+ than CS, replicating the other three experiments. Error bars are s.e.m. As detailed in the main text, the CS × phase interaction was significant. P < 0.01, two-tailed t-tests.

Extended Data Table 1 24-h retrieval memory results, mean proportion of responses
Extended Data Table 2 6-h retrieval memory results, mean proportion of responses
Extended Data Table 3 Immediate retrieval memory results, mean proportion of responses
Extended Data Table 4 Strong-encoding, 24-h retrieval memory results, mean proportion of responses

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Dunsmoor, J., Murty, V., Davachi, L. et al. Emotional learning selectively and retroactively strengthens memories for related events. Nature 520, 345–348 (2015) doi:10.1038/nature14106

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