Emotional arousal can produce lasting, vivid memories for emotional experiences, but little is known about whether emotion can prospectively enhance memory formation for temporally distant information. One mechanism that may support prospective memory enhancements is the carry-over of emotional brain states that influence subsequent neutral experiences. Here we found that neutral stimuli encountered by human subjects 9–33 min after exposure to emotionally arousing stimuli had greater levels of recollection during delayed memory testing compared to those studied before emotional and after neutral stimulus exposure. Moreover, multiple measures of emotion-related brain activity showed evidence of reinstatement during subsequent periods of neutral stimulus encoding. Both slow neural fluctuations (low-frequency connectivity) and transient, stimulus-evoked activity predictive of trial-by-trial memory formation present during emotional encoding were reinstated during subsequent neutral encoding. These results indicate that neural measures of an emotional experience can persist in time and bias how new, unrelated information is encoded and recollected.
This is a preview of subscription content
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
LaBar, K.S. & Cabeza, R. Cognitive neuroscience of emotional memory. Nat. Rev. Neurosci. 7, 54–64 (2006).
Phelps, E.A. & Sharot, T. How (and why) emotion enhances the subjective sense of recollection. Curr. Dir. Psychol. Sci. 17, 147–152 (2008).
Ochsner, K.N. Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. J. Exp. Psychol. Gen. 129, 242–261 (2000).
Kensinger, E.A. & Corkin, S. Memory enhancement for emotional words: are emotional words more vividly remembered than neutral words? Mem. Cognit. 31, 1169–1180 (2003).
Anderson, A.K., Wais, P.E. & Gabrieli, J.D.E. Emotion enhances remembrance of neutral events past. Proc. Natl. Acad. Sci. USA 103, 1599–1604 (2006).
Knight, M. & Mather, M. Reconciling findings of emotion-induced memory enhancement and impairment of preceding items. Emotion 9, 763–781 (2009).
McGaugh, J.L. Memory--a century of consolidation. Science 287, 248–251 (2000).
McGaugh, J.L. & Roozendaal, B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr. Opin. Neurobiol. 12, 205–210 (2002).
Phelps, E.A. Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr. Opin. Neurobiol. 14, 198–202 (2004).
Murty, V.P., Ritchey, M., Adcock, R.A. & LaBar, K.S. fMRI studies of successful emotional memory encoding: A quantitative meta-analysis. Neuropsychologia 48, 3459–3469 (2010).
Ritchey, M., Dolcos, F. & Cabeza, R. Role of amygdala connectivity in the persistence of emotional memories over time: an event-related FMRI investigation. Cereb. Cortex 18, 2494–2504 (2008).
Richardson, M.P., Strange, B.A. & Dolan, R.J. Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nat. Neurosci. 7, 278–285 (2004).
Popa, D., Duvarci, S., Popescu, A.T., Léna, C. & Paré, D. Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc. Natl Acad. Sci. USA 107, 6516–6519 (2010).
Dunsmoor, J.E., Murty, V.P., Davachi, L. & Phelps, E.A. Emotional learning selectively and retroactively strengthens memories for related events. Nature 520, 345–348(2015).
Hurlemann, R. et al. Noradrenergic modulation of emotion-induced forgetting and remembering. J. Neurosci. 25, 6343–6349 (2005).
Schwarze, U., Bingel, U. & Sommer, T. Event-related nociceptive arousal enhances memory consolidation for neutral scenes. J. Neurosci. 32, 1481–1487 (2012).
Packard, M.G. & Teather, L.A. Amygdala modulation of multiple memory systems: hippocampus and caudate-putamen. Neurobiol. Learn. Mem. 69, 163–203 (1998).
Roozendaal, B., Castello, N.A., Vedana, G., Barsegyan, A. & McGaugh, J.L. Noradrenergic activation of the basolateral amygdala modulates consolidation of object recognition memory. Neurobiol. Learn. Mem. 90, 576–579 (2008).
Strange, B.A., Hurlemann, R. & Dolan, R.J. An emotion-induced retrograde amnesia in humans is amygdala- and beta-adrenergic-dependent. Proc. Natl. Acad. Sci. USA 100, 13626–13631 (2003).
Segal, S.K., Stark, S.M., Kattan, D., Stark, C.E.L. & Yassa, M.A. Norepinephrine-mediated emotional arousal facilitates subsequent pattern separation. Neurobiol. Learn. Mem. 97, 465–469 (2012).
Henckens, M.J.A.G., Hermans, E.J., Pu, Z., Joëls, M. & Fernández, G. Stressed memories: how acute stress affects memory formation in humans. J. Neurosci. 29, 10111–10119 (2009).
van Marle, H.J.F., Hermans, E.J., Qin, S. & Fernández, G. Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. Neuroimage 53, 348–354 (2010).
Veer, I.M. et al. Beyond acute social stress: increased functional connectivity between amygdala and cortical midline structures. Neuroimage 57, 1534–1541 (2011).
Eryilmaz, H., Van De Ville, D., Schwartz, S. & Vuilleumier, P. Impact of transient emotions on functional connectivity during subsequent resting state: a wavelet correlation approach. Neuroimage 54, 2481–2491 (2011).
Sequeira, H., Hot, P., Silvert, L. & Delplanque, S. Electrical autonomic correlates of emotion. Int. J. Psychophysiol. 71, 50–56 (2009).
Rajaram, S. Remembering and knowing: two means of access to the personal past. Mem. Cognit. 21, 89–102 (1993).
Al-Aidroos, N., Said, C.P. & Turk-Browne, N.B. Top-down attention switches coupling between low-level and high-level areas of human visual cortex. Proc. Natl. Acad. Sci. USA 109, 14675–14680 (2012).
Norman-Haignere, S.V., McCarthy, G., Chun, M.M. & Turk-Browne, N.B. Category-selective background connectivity in ventral visual cortex. Cereb. Cortex 22, 391–402 (2012).
Duncan, K., Tompary, A. & Davachi, L. Associative encoding and retrieval are predicted by functional connectivity in distinct hippocampal area CA1 pathways. J. Neurosci. 34, 11188–11198 (2014).
Phelps, E.A. Emotion and cognition: insights from studies of the human amygdala. Annu. Rev. Psychol. 57, 27–53 (2006).
Hermans, E.J. et al. How the amygdala affects emotional memory by altering brain network properties. Neurobiol. Learn. Mem. 112, 2–16 (2014).
McGaugh, J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1–28 (2004).
Pitkänen, A., Pikkarainen, M., Nurminen, N. & Ylinen, A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann. NY Acad. Sci. 911, 369–391 (2000).
Saunders, R.C., Rosene, D.L. & Van Hoesen, G.W. Comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: II. Reciprocal and non-reciprocal connections. J. Comp. Neurol. 271, 185–207 (1988).
Stefanacci, L., Suzuki, W.A. & Amaral, D.G. Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 375, 552–582 (1996).
Fanselow, M.S. & Dong, H.-W. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7–19 (2010).
Dolcos, F., LaBar, K.S. & Cabeza, R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42, 855–863 (2004).
Touroutoglou, A., Hollenbeck, M., Dickerson, B.C. & Feldman Barrett, L. Dissociable large-scale networks anchored in the right anterior insula subserve affective experience and attention. Neuroimage 60, 1947–1958 (2012).
Uddin, L.Q., Kinnison, J., Pessoa, L. & Anderson, M.L. Beyond the tripartite cognition-emotion-interoception model of the human insular cortex. J. Cogn. Neurosci. 26, 16–27 (2014).
Kurth, F., Zilles, K., Fox, P.T., Laird, A.R. & Eickhoff, S.B. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 214, 519–534 (2010).
Chang, L.J., Yarkoni, T., Khaw, M.W. & Sanfey, A.G. Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb. Cortex 23, 739–749 (2013).
Yarkoni, T., Poldrack, R.A., Nichols, T.E., Van Essen, D.C. & Wager, T.D. Large-scale automated synthesis of human functional neuroimaging data. Nat. Methods 8, 665–670 (2011).
Rimmele, U., Lackovic, S.F., Tobe, R.H., Leventhal, B.L. & Phelps, E.A. Beta-adrenergic blockade at memory encoding, but not retrieval, decreases the subjective sense of recollection. J. Cogn. Neurosci. 28, 895–907 (2016).
Nielson, K.A., Yee, D. & Erickson, K.I. Memory enhancement by a semantically unrelated emotional arousal source induced after learning. Neurobiol. Learn. Mem. 84, 49–56 (2005).
Nielson, K.A. & Powless, M. Positive and negative sources of emotional arousal enhance long-term word-list retention when induced as long as 30 min after learning. Neurobiol. Learn. Mem. 88, 40–47 (2007).
Kensinger, E.A., Addis, D.R. & Atapattu, R.K. Amygdala activity at encoding corresponds with memory vividness and with memory for select episodic details. Neuropsychologia 49, 663–673 (2011).
Dougal, S., Phelps, E.A. & Davachi, L. The role of medial temporal lobe in item recognition and source recollection of emotional stimuli. Cogn. Affect. Behav. Neurosci. 7, 233–242 (2007).
Rimmele, U., Davachi, L., Petrov, R., Dougal, S. & Phelps, E.A. Emotion enhances the subjective feeling of remembering, despite lower accuracy for contextual details. Emotion 11, 553–562 (2011).
Kensinger, E.A., Garoff-Eaton, R.J. & Schacter, D.L. Effects of emotion on memory specificity: memory trade-offs elicited by negative visually arousing stimuli. J. Mem. Lang. 56, 575–591 (2007).
Mather, M. Emotional arousal and memory binding. Perspect. Psychol. Sci. 2, 33–52 (2007).
Stark, C.E.L. & Squire, L.R. When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc. Natl. Acad. Sci. USA 98, 12760–12766 (2001).
Lang, P.J., Bradley, M.M. & Cuthbert, B.N. International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (NIMH Center for the Study of Emotion and Attention, 1999).
Marchewka, A., Zurawski, Ł., Jednoróg, K. & Grabowska, A. The Nencki Affective Picture System (NAPS): introduction to a novel, standardized, wide-range, high-quality, realistic picture database. Behav. Res. Methods 46, 596–610 (2014).
Greicius, M.D., Krasnow, B., Reiss, A.L. & Menon, V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. USA 100, 253–258 (2003).
Damoiseaux, J.S. et al. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. USA 103, 13848–13853 (2006).
Avants, B.B., Epstein, C.L., Grossman, M. & Gee, J.C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 12, 26–41 (2008).
Behzadi, Y., Restom, K., Liau, J. & Liu, T.T. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37, 90–101 (2007).
Power, J.D., Barnes, K.A., Snyder, A.Z., Schlaggar, B.L. & Petersen, S.E. Steps toward optimizing motion artifact removal in functional connectivity MRI; a reply to Carp. Neuroimage 76, 439–441 (2013).
Power, J.D. et al. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84, 320–341 (2014).
Van Dijk, K.R.A., Sabuncu, M.R. & Buckner, R.L. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59, 431–438 (2012).
Power, J.D., Barnes, K.A., Snyder, A.Z., Schlaggar, B.L. & Petersen, S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142–2154 (2012).
Pruessner, J.C. et al. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cereb. Cortex 10, 433–442 (2000).
Fischl, B. et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355 (2002).
Maris, E. & Oostenveld, R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164, 177–190 (2007).
We thank E. Bar-David for expert assistance with data collection for the fMRI study and A. Patil, M. Kelemu, C. Brennan and D. Antypa for assistance with behavioral data collection. This work was supported by Dart Neuroscience (L.D.); NIMH grants MH074692 (L.D.), MH062104 (E.A.P.) and MH092055 (A.T.); and by grants from the Swiss National Science Foundation (PZ00P1_137126), the German Research Foundation (DFG RI 1894/2-1), and the European Community Seventh Framework Programme (FP7/2007-2013) under grant agreement 334360 to U.R.
The authors declare no competing financial interests.
Integrated supplementary information
Memory accuracy (hits minus false alarms) is shown for all hits (combined R and K responses, left bars), R responses (middle bars), and K responses (right bars) for both encoding orders (N=24 for E → N and N → E encoding orders, N=23 for N → N encoding order). Like the fMRI study (results shown in Fig. 2b), overall memory ((R+K)hits – (R+K)falsealarms) and recollection (Rhits – Rfalsealarms) for emotional vs. neutral stimuli significantly varied as a function of encoding order (Emotion by encoding order interaction, overall memory accuracy, F1,46 = 4.59, P =.037; R responses, F1,46 = 5.24, P =.027), with no reliable difference for Know responses (F1,46 =.38, P =.54). Overall memory and subjective recollection was greater for neutral stimuli encoded after emotional stimuli vs. neutral stimuli encoded before emotional stimuli (E → N vs. N → E encoding order; overall memory accuracy, t46 = 3.57, P =.00085; subjective recollection, t46 = 2.17, P =.035) as well as neutral stimuli encoded after neutral stimuli (E → N vs. N → N encoding order; see left and middle bars; overall memory accuracy, 1st block, t45 = 3.42, P =.0013, 2nd block, t45 = 4.22, P =.00015, permutation test, P =.0002; subjective recollection, 1st block, t45 = 2.59, P =.013, 2nd block, t45 = 3.24, P =.0023). Memory for emotional stimuli did differ as a function of encoding order for overall memory accuracy (t46 = 2.48, P =.017) but not for subjective recollection (t46 =.55, P =.58). The only qualitative difference between these data and those in the fMRI study is that a memory benefit was found for emotional vs. neutral stimuli in the E-N encoding order (overall memory accuracy, t23 = 2.43, P =.023; subjective recollection, t23 = 2.83, P =.0095; compare with Fig. 2b). All error bars in all figures represent standard error of the mean across subjects. The N→N encoding order data are the same as in Fig. 2b and are presented again for comparison with the E → N behavioral group. *P <.05, **P <.005
Supplementary Figure 2 Low-frequency connectivity in the ventral anterior insula network as a function of encoding order.
(a). The ventral Anterior Insula (vAI) network was defined from the first rest scan, prior to any encoding blocks. This network was defined as regions showing reliable correlation with a seed region in the right vAI and consisted of the bilateral vAI, medial prefrontal cortex, and posterior cingulate cortex (regions shown in red).
(b). Low-frequency connectivity in this network as a function of encoding order (N = 20 for each encoding order). Note that the pattern of results mirrors the results found for amygdala – anterior hippocampal LF connectivity (Fig. 4b). A significant interaction was found between encoding order and emotional vs. neutral encoding (F1,38 = 6.47, P =.015). Connectivity differed between emotional and neutral encoding in the N → E encoding order (when no ‘carry-over’ of emotion into neutral encoding could be present; t19 = 3.09, P =.006), but not the E → N encoding order (when emotion could ‘carry-over’ into neutral encoding; t19 = -.32, P =.75). A trend (t38 = 1.86, ~P =.071) was found for greater connectivity during neutral encoding when neutral stimuli were encountered after vs. before emotional stimuli (in the E → N vs. the N → E encoding order), but connectivity did not differ during emotional encoding as a function of encoding order (t38 =.014, P =.99). *P <.05
Supplementary Figure 3 Nonparametric significance test of difference in similarity of emotional and neutral patterns related to subsequent recollection memory as a function of encoding order.
To non-parametrically assess the significance of enhanced whole-brain similarity of patterns related to subsequent recollection of emotional and neutral stimuli when neutral stimuli were encoded after vs. before emotional stimuli (shown in Fig. 5, greater similarity in the E → N vs. N → E encoding order), null simulations were performed (N = 1,000) in which the subsequent memory labels of individual trials were randomly shuffled in each condition (emotional and neutral encoding) per subject, and the similarity of emotional and neutral encoding-related patterns (R minus K activity estimates) was computed. This histogram shows the null distribution of the difference in the similarity of encoding-related (R minus K activity estimates) multi-voxel patterns between emotional and neutral encoding as a function of encoding order (E → N minus N → E pattern similarity). The red line indicates the true difference (.08) in pattern similarity, which is significant relative to this null distribution (P =.00083). Since the conditions of interest (subsequent memory labels) are shuffled within each condition per subject, these null simulations inherently account for differences in bin sizes for R and K trials across conditions that are present as a function of encoding order.
Supplementary Figure 4 Anterior–posterior localization of hippocampal subsequent recollection-based memory effects as a function of encoding order.
Anterior-posterior localization (bias scores) of Hippocampal recollection-based encoding effects (voxels showing R > K activity) were computed during emotional and neutral encoding as a function of encoding order for each participant (N=21 for each encoding order). The anterior-posterior bias score indicates the average location of voxels showing encoding effects related to subsequent recollection (R > K activity estimates) along the long axis of the hippocampus (scored from +1 for the most anterior hippocampal slice and -1 for the most posterior slice). Subsequent recollection bias scores showed a marginal difference between emotional and neutral encoding based on encoding order (Emotion by encoding order interaction, F1,40 = 2.95, P =.094; permutation test, P =.096). Similar anterior vs. posterior biases of subsequent recollection effects were found during emotional and neutral encoding for the E → N encoding order (in which emotional arousal could ‘carry-over’ into neutral encoding, left bars, t20 = -.32, P =.75; permutation test, P =.755). However, significantly greater anterior vs. posterior bias scores (more anterior localization of voxels showing recollect-based encoding effects) were found in emotional vs. neutral encoding for the N → E encoding order (when no ‘carry-over’ of emotional arousal could be present during neutral encoding; t20 = 2.16, P =.043; permutation test, P =.0396). Moreover, hippocampal voxels supporting subsequent recollection were more anteriorly localized when neutral stimuli were encountered after vs. before emotional stimuli (red vs. blue bar; t40 = 2.20, P =.034; permutation test, P =.037), with no difference in location for emotional stimuli as a function of encoding order (t40 =.002, P =.998; permutation test, P =.99). *P <.05
About this article
Cite this article
Tambini, A., Rimmele, U., Phelps, E. et al. Emotional brain states carry over and enhance future memory formation. Nat Neurosci 20, 271–278 (2017). https://doi.org/10.1038/nn.4468
Impact of music-based intervention on verbal memory: an experimental behavioral study with older adults
Cognitive Processing (2021)
Psychological Research (2021)
Scientific Reports (2020)
Exams at classroom have bidirectional effects on the long-term memory of an unrelated graphical task
npj Science of Learning (2018)
Nature Reviews Neuroscience (2017)