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.
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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
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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
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