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. Author manuscript; available in PMC: 2026 Mar 12.
Published in final edited form as: Nat Neurosci. 2016 Dec 26;20(2):271–278. doi: 10.1038/nn.4468

Emotional brain states carry over and enhance future memory formation

Arielle Tambini 1,6, Ulrike Rimmele 2,6, Elizabeth A Phelps 3,4,5, Lila Davachi 3,4
PMCID: PMC12977101  NIHMSID: NIHMS2138028  PMID: 28024158

Abstract

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.

We form lasting, vivid and detailed memories for only a subset of our experiences. Emotion is one key factor that influences the fate of our memories1,2. Compared to their neutral counterparts, emotional events and stimuli are more robustly remembered, with higher levels of confidence, vividness and detail1-4. The presence of emotion not only increases recollection of emotionally arousing experiences themselves but also has been shown to retroactively modulate recollection of neutral information preceding emotional arousal5,6. Despite such findings documenting the impact of emotion on memory for information before and during manipulations of emotional arousal, little work has examined whether emotion can prospectively enhance memory for subsequently encountered information minutes later. Moreover, it is unknown whether the persistence of emotional arousal is capable of impacting future brain states and modifying the neural structures that support memory formation for subsequently encountered stimuli. Here we assessed whether exposure to emotionally arousing stimuli prospectively enhances memory for subsequently encountered stimuli by biasing future states of brain activity.

A robust body of literature indicates that emotional arousal during an experience enhances the consolidation of memory for that particular event, resulting in more persistent, vivid and detailed emotional memories over time1-4. Mechanistically, emotional arousal has been linked with the release of norepinephrine and epinephrine, which, in concert with the amygdala, are thought to modulate hippocampal processes during both the encoding and subsequent consolidation of emotional experiences1,7-9. Supporting this notion, activity within and connectivity between the amygdala, hippocampus and medial temporal lobe cortex reliably predicts successful emotional memory formation and consolidation10-13. In addition to enhancing memory for emotional events themselves, emotional learning and exposure to emotional stimuli—or the induction of arousal pharmacologically or with shock—can retroactively enhance long-term retention of preceding neutral information5,6,14-18 (but see refs. 15,19).

But what about unrelated neutral information that follows an emotional experience? Can extended periods of emotional arousal bias future brain states and, in doing so, prospectively modify the neural structures supporting memory formation for unrelated, neutral information? Prior work has examined the influence of emotion on memory for information encountered seconds after emotional arousal6,15,19, and a recent study found that individual differences in arousal induced by a block of emotional stimuli were related to enhanced memory discrimination for similar visual images presented a few minutes later20. Previous studies have also examined the impact of stress on memory formation for both emotional and neutral stimuli. Memory for both emotional and neutral images is enhanced when encoding blocks are interleaved with a stress manipulation21. At the neural level, amygdala connectivity remains altered after stress induction22-24, and stress induction can alter activation in brain regions related to memory formation for both emotional and neutral stimuli21. However, to our knowledge, no prior investigations have examined how extended periods of emotional arousal can prospectively bias future brain states and thereby modify the manner in which unrelated, neutral information is encoded into memory. Here, we tested whether arousal and brain states associated with an extended (~20 min) emotional experience can carry-over and bias the encoding of neutral stimuli encountered approximately 9 to 33 min later and thereby modulate how those stimuli are encoded into memory (Fig. 1).

Figure 1.

Figure 1

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Experimental design and predictions. (a) Experimental design: separate groups of subjects performed blocks of incidental emotional and neutral encoding (E→N, subjects that performed emotional followed by neutral encoding; N→E, subjects that performed neutral followed by emotional encoding): two groups encoded stimuli during fMRI scanning (E→N and N→E encoding orders), while two other groups of subjects underwent E→N and N→E encoding blocks under behavioral testing conditions (Supplementary Fig. 1) and one other group encoded neutral stimuli outside of the context of emotional stimuli under behavioral testing conditions (N→N). Encoding blocks were separated by rest periods (cream boxes). (b) We predicted that arousal associated with emotional encoding would persist and carry over, prospectively biasing brain activity during subsequent neutral (neu) encoding and enhancing memory for neutral stimuli for the E→N encoding order. No emotional bias or carry-over of emotion should be present in the other encoding orders. A prospective influence of emotion on subsequent neutral encoding predicts that several factors listed should be differentially present during neutral encoding for the E→N vs. N→E encoding order (greater memory, arousal, emotion-related activity and neural pattern similarity between emotional and neutral encoding).

To this end, two groups of subjects underwent blood-oxygen-level-dependent (BOLD) functional MRI (fMRI) scanning during incidental encoding of extended (23 min) blocks of emotional and neutral complex scenes (emotional and neutral encoding conditions; Fig. 1a), returning 6 h later for a surprise memory test. One group of subjects first encountered an extended block of emotional stimuli followed by neutral stimuli (‘E-N encoding order’), while a different group of subjects encountered neutral stimuli followed by emotional stimuli (‘N-E encoding order’). A separate group of subjects incidentally encoded blocks of neutral stimuli under the same procedures as the fMRI subjects (but outside of the MRI scanner), and two other groups of subjects incidentally encoded blocks of emotional and neutral stimuli (E-N and N-E encoding orders) outside of the MRI scanner (Fig. 1a). We reasoned that the prospective influence of emotion, or a carry-over of an emotional state into subsequent neutral encoding, should be present when subjects encoded a long block of emotional stimuli first and neutral stimuli second (E-N encoding order) but not for the opposite encoding order (N-E encoding order) or when only neutral stimuli were encoded outside of the context of emotional stimuli (N-N encoding order). We first assessed the persistence of emotional arousal from emotional encoding into subsequent neutral encoding blocks by measuring skin conductance levels (SCL) as a proxy for sympathetic nervous system activation25 Behaviorally, we asked whether the carry-over of an emotional state would enhance the subjective recollection of subsequently encountered neutral stimuli (in the E-N encoding order relative to the other encoding orders). Finally, using fMRI, we examined whether emotion would prospectively bias future encoding-related brain activity in at least two ways (Fig. 1b): first, we asked whether BOLD activity patterns during emotional and neutral encoding were more similar when neutral stimuli were encoded after versus before emotional stimuli (E-N versus N-E encoding order) and second, whether brain regions supporting emotional memory (for example, amygdala and anterior hippocampus) were more active and showed greater levels of connectivity when neutral stimuli were encoded after versus before emotional stimuli (i.e., when a carry-over of emotional arousal may have been present).

RESULTS

Skin conductance

If emotional arousal following an extended block of emotional encoding persists into neutral encoding, then overall SCL, which is related to sympathetic nervous system activation25, should track this persistence and differ based on emotion and encoding order. To account for individual differences in baseline skin conductance, SCL was computed as the change relative to a baseline rest period obtained before the first encoding block (referred to as ‘relative SCL’; Online Methods). When assessing relative SCL in the fMRI study, we found a significant interaction between emotion (emotional versus neutral encoding) and encoding order (Fig. 2a; F1,42 = 8.72, P = 0.0051; permutation test, P = 0.0036). Elevated SCL showed evidence of persistence from long-lasting blocks of emotional into subsequent neutral encoding (Fig. 2a). Specifically, SCL increased during emotional encoding compared to the preceding baseline rest scan (t21 = 3.21, corrected P = 0.0167; permutation test, corrected P = 0.004) and remained heightened during a block of subsequent neutral encoding (SCL relative to baseline rest scan, t21 = 3.06, corrected P = 0.0239; permutation test, corrected P = 0.0096). Thus SCL levels were equivalent between emotional and neutral encoding when neutral stimuli were encoded tens of minutes after emotional stimuli (E-N encoding order, t21 = 0.51, P = 0.61; permutation test, P = 0.65), despite the temporal separation of these encoding blocks. By contrast, SCL was significantly greater during emotional versus neutral encoding when neutral stimuli were encoded before emotional stimuli (N-E encoding order; Fig. 2a; t21 = 3.19, P = 0.0044; permutation test, P = 0.0022).

Figure 2.

Figure 2

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Skin conductance levels and behavioral results. (a) Mean galvanic SCLs are shown for each encoding order in the fMRI study (n = 22 for each N→E and E→N encoding order) and for the N→N encoding order for the behavioral study (n = 23), with each data point representing data from each subject. Larger (filled) data points indicate means across subjects. SCL is plotted relative to each subjects’ baseline SCL during the first rest period. Each encoding block (emotional, emo; neutral, neu) has three measurements, corresponding to the mean relative SCL during three encoding scans (or 7.7 min epochs) for that block. Asterisks above data points denote significant differences in SCL from the first baseline rest scan (corrected for multiple comparisons in each encoding order). (b) Memory was assessed for stimuli seen during encoding using a remember (R)–know (K) procedure. 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 the fMRI study (E→N and N→E encoding orders; n = 22 for each encoding order) and the N→N encoding order (behavioral study, n = 23). See Supplementary Figure 1 for similar results for E→N and N→E encoding orders in the behavioral study. All error bars represent s.e.m. across subjects and individual dots represent data from each subject. ~P = 0.053, *P < 0.05, **P < 0.005.

We next directly tested whether relative SCL during neutral encoding was enhanced when neutral stimuli were encountered after emotional stimuli, compared to before emotional stimuli (N-E encoding order) or after neutral stimuli (N-N encoding order). Relative SCL during neutral encoding was marginally enhanced for E-N versus N-E (t42 = 1.62, P = 0.056, one-tailed t-test; one-tailed permutation test, P = 0.053) and N-N encoding orders (comparison with second block, t43 = 1.32, P = 0.097, one-tailed t-test; one-tailed permutation test, P = 0.098; comparison with first block, t43 = 1.50, P = 0.071, one-tailed t-test; one-tailed permutation test, P = 0.073). However, relative SCL during emotional encoding did not differ between encoding orders (t42 = 0.82, P = 0.42; permutation test, P = 0.41). These results provide evidence for enhanced SCL when neutral stimuli were encountered after emotional stimuli, supporting the notion that a block of emotional stimuli can induce arousal that persists tens of minutes later, into and during an extended block of subsequent neutral encoding.

Memory performance

Next, we compared memory for neutral stimuli as a function of encoding order, to assess whether a long block of emotionally arousing stimuli is capable of prospectively enhancing memory for neutral stimuli encountered 9 to 33 min later. Memory for stimuli encountered during the encoding sessions was assessed in a surprise memory test 6 h later using a remember (R)–know (K) procedure26. We first assessed whether emotional and neutral memory differed based on encoding order in the fMRI study (reported below), as well as in separate groups of behavioral participants that did not undergo fMRI scanning (Supplementary Fig. 1). As expected, overall memory accuracy (proportion of total R and K hits minus false alarms) was higher for emotional versus neutral stimuli (main effect of emotion: F1,42 = 16.0, P = 0.00025). However, memory accuracy differed as a function of encoding order (Fig. 2b and Supplementary Fig. 1; encoding order by emotion interaction: F1,42 = 10.6, P = 0.0022). As in the SCL data reported above, no reliable difference in emotional versus neutral memory was found in the fMRI study when neutral stimuli were encountered after emotional stimuli (E-N encoding order; Fig. 2b; t21 = 0.66, P = 0.52), during which emotional arousal showed evidence of persistence into subsequent neutral encoding (via enhanced SCL; Fig. 2a). However, a robust enhancement in emotional memory was found for the opposite N-E encoding order (Fig. 2b; t21 = 4.37, P = 0.00027), in which no carry-over of emotional arousal could be present. Our main question concerned whether exposure to extended blocks of emotionally arousing stimuli could prospectively enhance memory for neutral stimuli encountered tens of minutes later. Memory for neutral stimuli was significantly greater when they were encoded after versus before emotional stimuli and outside of the context of emotional stimuli (Fig. 2b and Supplementary Fig. 1): corrected recognition rates of 62.7% were found in the E-N encoding order compared to 53.5% in the N-E encoding order (t42 = 2.06, P = 0.045) and 52.0% and 46.5% in the N-N encoding order (first and second blocks of N-N encoding order; first block, t43 = 2.41, P = 0.02; second block, t43 = 3.31, P = 0.002; permutation test, P = 0.0022). In contrast to neutral stimuli, memory accuracy for emotional stimuli did not differ between E-N and N-E encoding orders (Fig. 2b; t42 = −0.78, P = 0.44). Note that the same pattern of results was observed in separate behavioral groups, with enhanced levels of memory for neutral stimuli when they were encountered after emotional stimuli (E-N encoding order) relative to the other encoding orders (Supplementary Fig. 1). These results demonstrate that emotion can prospectively enhance memory for neutral stimuli encountered tens of minutes later.

Given prior work indicating that emotion specifically enhances the subjective sense of recollection (for example, see ref. 3) we asked whether the memory benefit for neutral stimuli encountered after emotional encoding blocks showed the same specificity. Comparing emotional and neutral memory based on encoding order in the fMRI study, a significant triple interaction was found between R versus K responses, emotional versus neutral stimuli and encoding order (F1,42 = 14.0, P = 0.0006). As predicted, R responses differed for emotional versus neutral stimuli based on encoding order (emotion by encoding order interaction: F1,42 = 20.7, P = 4.5 × 10−5; Fig. 2b and Supplementary Fig. 1). Consistent with a carry-over or persistence of emotional arousal into subsequent neutral encoding, levels of emotional and neutral R responses were similar when neutral stimuli were encountered after emotional stimuli in the fMRI study (E-N encoding order; Fig. 2b; t21 = 0.49, P = 0.63). However, in the opposite N-E encoding order, R responses were significantly higher for emotional compared to neutral stimuli (Fig. 2b; t21 = 5.99, P = 6 × 10−6). Crucially, similar to the combined memory measure reported above, R responses were significantly greater for neutral stimuli when they were encountered after versus before long blocks of emotional stimuli (Fig. 2b and Supplementary Fig. 1; t42 = 2.16, P = 0.037) and versus neutral stimuli in the N-N encoding order (Fig. 2b and Supplementary Fig. 1; first block, t43 = 2.20, P = 0.03; second block, t43 = 2.87, P = 0.006). This enhancement in neutral R responses was found for both the fMRI study (reported here) and the behavioral participants (Supplementary Fig. 1). However, in contrast to neutral stimuli, R responses for emotional stimuli did not reliably differ across E-N and N-E encoding orders (t21 = −1.38, P = 0.17; Fig. 2b and Supplementary Fig. 1). In contrast to recollection-based R responses, K responses did not significantly differ for neutral versus emotional stimuli across encoding orders (Fig. 2b and Supplementary Fig. 1; emotional stimuli, t42 = 0.97, P = 0.34; neutral stimuli, t42 = −0.48, P = 0.64; emotion by encoding order interaction, P = 0.09).

The above results indicate that subjective recollection of neutral stimuli was relatively greater when they were encountered 9 to 33 min after blocks of emotional stimuli, mirroring enhanced SCL found during neutral encoding. In contrast to differences in neutral memory and SCL during neutral encoding, levels of subjective recollection and SCL during emotional encoding did not consistently differ as a function of encoding order. This pattern of results was observed in two independent data sets (during fMRI scanning and in a separate behavioral study). Together, these findings are consistent with the notion that long-lasting blocks of emotional arousal can persist on an extended timescale and prospectively enhance the later recollection of neutral stimuli encountered at least 9 to 33 min later.

Low-frequency connectivity carry-over effects

Next, we sought to examine evidence for the hypothesis that exposure to long blocks of emotional stimuli created a specific, arousal-related brain state that could bias subsequent BOLD activity patterns during neutral encoding. Given the extended time period of the encoding sessions (~23 min) as well as the temporal gap between emotional and neutral encoding (~9 min), the carry-over of such an emotional brain state may have occurred at a relatively slow timescale (for example, on the order of minutes). Thus, we reasoned that this brain state might be manifest in low-frequency (LF) fluctuations in the BOLD signal, i.e., BOLD signal changes that were slower than trial-by-trial evoked activity. Such slow LF fluctuations have previously been shown to track different behavioral states27-29. To test this hypothesis, we examined whether patterns of LF connectivity that characterized emotional encoding blocks carried over or showed evidence of reinstatement during subsequent neutral encoding blocks (Fig. 3a).

Figure 3.

Figure 3

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Low-frequency connectivity as a function of encoding order. (a) Low frequency connectivity analysis approach. Left: plot shows the power spectrum of amygdala BOLD encoding data for an example subject. A peak in the power spectrum can be seen for the task frequency, 0.0714 Hz. To examine LF connectivity, BOLD data were filtered below 0.06 Hz. Right: plot shows LF filtered time courses of amygdala and anterior hippocampus BOLD data from one subject during emotional encoding. (b) Similarity of multivoxel LF amygdala connectivity patterns between emotional and neutral encoding blocks as a function of encoding order. Example data from one subject from the E→N encoding order (top left) and one subject from the N→E encoding order (bottom left) are shown. An example amygdala ROI (used as the seed region) is shown in the left inset. Images show sagittal slices containing LF connectivity patterns with the amygdala. Vectors next to each image depict the analysis approach; the similarity of multivoxel connectivity patterns in each subject was computed between emotional and neutral encoding blocks. Right plot shows group data (n = 20 subjects in each encoding order) for the similarity of multivoxel LF amygdala correlation patterns between emotional and neutral encoding. Individual data points represent the similarity (correlation) for each subject. Error bars, s.e.m. *P < 0.05

Given the importance of the amygdala in mediating the influence of emotion on memory and cognition30-32, we asked whether large-scale patterns of LF amygdala connectivity representative of an emotional brain state showed evidence of reinstatement during neutral encoding blocks. Such reinstatement would result in greater similarity between emotional and neutral encoding LF amygdala connectivity patterns when neutral stimuli are encountered after versus before emotional stimuli (E-N versus N-E encoding order). To this end, we computed LF connectivity across cortical and subcortical voxels using the amygdala as a seed region. Connectivity was computed separately for each encoding scan in each subject, resulting in distinct multivariate images or vectors representing LF amygdala connectivity patterns during emotional and neutral encoding (Fig. 3b). We then asked whether these global patterns of LF amygdala connectivity were more similar (i.e., exhibited higher levels of correlation) between emotional and neutral encoding blocks for the E-N encoding order (in which a carry-over of emotional arousal into subsequent neutral encoding was found) versus the N-E encoding order (in which no carry-over of emotional arousal should be present). LF amygdala connectivity patterns were significantly more correlated (i.e., more similar) during emotional and neutral encoding for the E-N versus the N-E encoding order (Fig. 3b; t38 = 2.42, P = 0.02). This result indicates that large-scale, multivoxel patterns of LF amygdala connectivity representative of emotional encoding can carry over and manifest tens of minutes later when unrelated neutral stimuli are later encountered.

At a more fine-grained level, we next examined specific interactions between the amygdala and anterior hippocampus, which are thought to underlie the memory benefit for emotional stimuli9,12,32. We targeted the anterior hippocampus since it is expected to show the strongest interactions with the amygdala, based on anatomy33-36 and prior reports of functional correlations between amygdala and anterior hippocampal BOLD activity37 and since anterior hippocampal activation is consistently predictive of successful emotional encoding10. As shown in Figure 4, levels of LF amygdala–anterior hippocampal connectivity also showed evidence of being reinstated or carrying over from emotional to neutral encoding blocks. First, connectivity during emotional versus neutral encoding differed as a function of encoding order (emotion by encoding order interaction, F138 = 4.57, P = 0.039). Mirroring our behavioral and SCL findings, similar levels of LF amygdala–anterior hippocampal connectivity were found during emotional and neutral encoding when neutral stimuli were encountered tens of minutes after emotional stimuli (E-N encoding order, t19 = −0.82, P = 0.42), but a significant enhancement in LF connectivity was found during emotional versus neutral encoding for the opposite encoding order (N-E encoding order, t19 = 2.12, P = 0.048). Moreover, LF amygdala–anterior hippocampal connectivity was significantly greater during neutral encoding blocks when neutral stimuli were encountered after versus before emotional stimuli (E-N versus N-E encoding orders; t38 = 2.38, P = 0.023). Yet no reliable difference in connectivity was found during emotional encoding blocks between encoding orders (t38 = 0.97, P = 0.34). This pattern of results suggests that LF amygdala–anterior hippocampal connectivity, like overall levels of skin conductance, showed evidence of carrying over from temporally extended blocks of emotional encoding into subsequent neutral encoding.

Figure 4.

Figure 4

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Low-frequency amygdala–anterior hippocampal connectivity as a function of encoding order. (a) Anatomically defined amygdala (red) and anterior hippocampus (blue) ROIs are shown for an example subject. (b) LF amygdala–anterior hippocampus connectivity as a function of encoding order across n = 20 subjects per encoding order. LF amygdala–anterior hippocampal connectivity is greater during neutral encoding for the E→N vs. N→E encoding order (red vs. blue bars). Individual data points represent connectivity for each subject. Error bars, s.e.m. *P < 0.05.

Lastly, we found similar evidence for a carry-over effect in levels of LF connectivity from emotional into neutral encoding within the ventral anterior insula (vAI) network (Supplementary Fig. 2). We additionally probed connectivity in this network as emotion-related activity has consistently been shown in the vAI (refs. 38-41), and greater levels of vAI network connectivity have been related to heightened arousal ratings of the emotional stimuli used in this experiment38.

Taken together, these results provide evidence that emotional brain states, measured by correlations in LF BOLD fluctuations present during emotional encoding, can carry-over and become reinstated tens of minutes later when participants encountered unrelated, neutral information. Multiple signatures of emotion-related LF connectivity showed evidence of carrying over from emotional encoding into subsequent neutral encoding and were present in both local networks (for example, amygdala–anterior hippocampal connectivity) and in global pattern similarity across the brain (in multivoxel amygdala connectivity patterns).

Event-related subsequent memory carry-over effects

In addition to asking whether correlations in LF fluctuations in the BOLD signal showed evidence of carry-over from blocks of emotional to subsequent neutral encoding, we also examined whether emotional encoding prospectively influenced transient, stimulus-evoked or event-related BOLD activity during subsequent exposure to neutral stimuli. Given our data suggesting that emotion prospectively enhanced behavioral signatures of memory for subsequently encountered neutral stimuli, we asked whether the neural structures supporting memory formation for neutral stimuli were modulated on a trial-by-trial basis by the prior induction of an emotional state. Specifically, we compared stimulus-evoked activity related to subsequent recollection-based memory (i.e., greater activation for stimuli later labeled as R versus K) during emotional and neutral encoding blocks based on the order of encoding blocks, using both univariate and multivariate approaches. As a function of encoding order, we compared (i) the similarity of global, multivoxel patterns supporting later recollection between emotional and neutral encoding and (ii) univariate activation predicting subsequent recollection between emotional and neutral encoding.

First, we asked whether global, multivoxel patterns that characterize recollection-based emotional memory formation were reinstated and similarly supported the later recollection of neutral stimuli encountered after emotional stimuli. Such a reinstatement would result in greater similarity between multivoxel patterns supporting later recollection during emotional and neutral encoding when neutral stimuli are encountered after versus before emotional stimuli. To test this prediction, we measured activation patterns related to successful recollection-based memory formation (differences in activation estimates for trials later labeled as R versus K) separately for emotional and neutral stimuli in each participant (Fig. 5a). This resulted in multivoxel activity patterns across cortical and subcortical voxels that were characteristic of recollection-based memory formation, which we then compared between emotional and neutral stimuli as a function of encoding order. Enhanced levels of similarity, or correlation, were found between multivoxel patterns supporting recollection-based memory for emotional and neutral stimuli when neutral stimuli were encountered after versus before emotional stimuli (in the E-N versus N-E encoding order; Fig. 5b; t40 = 3.00, P = 0.0046). A nonparametric permutation test was performed to ensure that this difference in multivoxel pattern similarity was not driven by differences in R versus K bin sizes between encoding orders (P = 0.00083; Supplementary Fig. 3). This result demonstrates that spatially broad activation patterns related to recollection-based memory formation were more similar between emotional and neutral stimuli when neutral stimuli were encountered after versus before emotional encoding blocks. This result suggests that patterns of brain activity supporting successful recollection-based memory formation of neutral stimuli were prospectively biased by the presence of prior emotional stimuli tens of minutes earlier, with activation patterns supporting later neutral stimulus recollection being more similar to emotional encoding patterns when neutral stimuli were preceded by emotional stimuli.

Figure 5.

Figure 5

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Similarity of multivoxel subsequent recollection-based memory differences between emotional and neutral encoding as a function of encoding order. (a) Example data are shown from one subject of the E→N encoding order (top) and one subject of the N→E encoding order (bottom). Sagittal slices depict subsequent recollection patterns (R – K activity estimates) across cortical and subcortical voxels. (b) Group data for the similarity of multivoxel encoding patterns (activity patterns supporting subsequent recollection memory (SRM)) between emotional and neutral encoding based on encoding order (n = 21 subjects per encoding order). Greater similarity of patterns supporting subsequent emotional and neutral recollection was found for the E→N vs. N→E encoding orders for both global patterns across cortical and subcortical voxels (whole-brain, left bar plot) and within the hippocampus (right bar plot). Individual data points represent similarity (correlation) for each subject. Error bars, s.e.m. *P < 0.05, **P < 0.005.

Next, we examined whether similar effects were found within the hippocampus, as emotion is thought to enhance recollection-based memory formation via hippocampal mechanisms1,7-9. Hippocampal activity patterns showed evidence of carry-over effects or reinstatement of activity patterns representative of emotional encoding during subsequent neutral encoding blocks, both in multivoxel patterns predictive of later recollection (Fig. 5b; t40 = 2.02, P = 0.049) and in the anterior versus posterior localization of hippocampal voxels contributing to subsequent recollection36,37 (Supplementary Fig. 4 and Online Methods). These findings indicate that patterns of hippocampal activity supporting recollection-based memory formation of neutral stimuli were also biased by the presence of prior emotion, specifically by enhancing the contribution of the anterior hippocampus to memory formation.

Lastly, we asked whether individual brain regions supporting successful recollection-based memory formation were more similar between emotional and neutral stimuli when neutral stimuli were encountered after emotional stimuli than when neutral stimuli were encountered before emotional stimuli. To this end, we identified regions that showed significant subsequent recollection effects (R > K BOLD responses) for emotional stimuli as well as greater R > K activity when neutral stimuli were encountered after versus before emotional stimuli (E-N versus N-E encoding order). This carry-over recollection-based memory effect was operationalized as brain regions that showed a conjunction between six contrasts, depicted in Figure 6a (Online Methods; note that this analysis also controls for differences in R and K bin sizes based on encoding order). Six regions emerged from this whole brain conjunction analysis (Fig. 6b; family-wise error (FWE)-corrected, P < 0.05): the left amygdala, the right perirhinal cortex, the right posterior inferior temporal gyrus and three regions in bilateral inferior prefrontal cortex. Similar regions have previously been shown to predict successful memory formation for emotional versus neutral stimuli10, and a formal decoding analysis performed on the uncor-rected conjunction map revealed the highest similarity with terms “emotional stimuli,” “affect” and “salient” (using neurosynth.org42, http://neurosynth.org/decode/?neurovault=JOYXPMRX-26012). Here we found that regions associated with emotional processing and memory formation were predictive of subsequent neutral memory when neutral stimuli were encountered after, but not before, extended blocks of emotional stimuli. The engagement of these additional brain regions subserving neutral memory formation after emotional arousal supports the idea that emotion- and encoding-related mechanisms were reinstated and thus impacted memory formation 9 to 33 min later.

Figure 6.

Figure 6

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Subsequent recollection-based memory carry-over effects. (a) Schematic of response patterns required for a subsequent recollection carry-over effect, or reinstatement of emotional subsequent recollection effects during later neutral encoding (six-way conjunction analysis). Regions showed significant subsequent recollection effects or significantly greater activity estimates for R vs. K trials during emotional encoding (both encoding orders) and neutral encoding when neutral stimuli were encountered after emotional stimuli (E→N encoding order, red bars). Regions also showed significantly greater R – K differences between the three conditions with arrows. Individual contrasts were thresholded at *P < 0.05. (b) Brain regions showing emotional subsequent recollection effects that carry over during later neutral encoding, isolated from the conjunction analysis shown in a. Six regions emerged from this analysis (shown in red): left amygdala (P = 0.013), right perirhinal cortex (P = 0.004), left inferior temporal (IT) cortex (P = 0.0088) and three inferior prefrontal cortex (PFC) regions (two shown; left P = 0.0006, right P = 0). Results are FWE-corrected at P < 0.05, and the resulting map was smoothed for visualization. Statistical map is displayed on the group template anatomical image and can be found in MNI space on neurovault.org (http://neurovault.org/collections/JOYXPMRX/).

DISCUSSION

It is widely acknowledged that emotion can modulate what and how we remember. Although prior work has shown that emotion can retroactively influence memory for preceding neutral experiences5,6,14,15, less is known about how emotional experiences can linger and prospectively enhance memory formation for neutral information encountered many minutes later. We found that exposure to extended blocks of emotion-evoking stimuli induced a lasting emotional state that enhanced participants’ later recollection of neutral images encountered 9 to 33 min later, suggesting that the impact of emotion carried over into and biased subsequent stimulus processing and encoding. We directly queried the persistence or carry-over of an emotional brain state into subsequent neutral encoding blocks by analyzing global multivoxel patterns across the brain and activity in emotion- and arousal-related brain regions. First, we found that LF fluctuations of the BOLD signal previously shown to track behavioral or neural states27-29 carried over from emotional encoding into subsequent neutral encoding blocks. These included global multi voxel amygdala–whole-brain connectivity patterns, as well as correlated activity in targeted circuits (amygdala–anterior hippocampus and ventral anterior insula network). Second, we found that brain regions exhibiting successful encoding effects for neutral stimuli were also modulated by preceding emotional experiences. Thus, both large-scale patterns and overall levels of BOLD activity supporting recollection-based memory formation were reinstated during neutral encoding after emotional encoding blocks. Together, these findings provide evidence that the induction of a relatively lasting emotional state was associated with brain states that could later be reinstated, biasing the way future neutral events were encoded and potentially imbuing neutral experiences with emotional properties that enhance their recollection.

Previous studies of emotion’s influence on memory have demonstrated that the neurohormonal changes underlying physiological arousal are critical for mediating emotion-enhanced memory7,8, specifically subjective recollection43, although these might not be the only contributing factors. In the present study, we induced an emotional state through the use of stimuli previously rated as subjectively negative and arousing (compared to stimuli rated as neutral). We then used SCL, a noninvasive assessment of autonomic arousal, as our primary measure of emotion25. Notably, increased levels of emotional arousal induced by the exposure to emotional stimuli persisted in time and likely influenced the encoding, and perhaps consolidation, of subsequently encountered neutral stimuli, resulting in increased levels of subjective recollection when the neutral memory was assessed 6 h later. This enhancement in recollection of neutral stimuli was observed across two independent data sets. Crucially, mirroring our behavioral findings, SCL was distinctly higher when neutral stimuli were encountered 9 to 33 min after emotional stimuli versus before emotional stimuli as well as after neutral stimuli. For these reasons, together with prior evidence linking emotion-related neurohormonal changes with subjective recollection43, we believe the subsequent influence of emotion on memory for future neutral events may be mediated by noradrenergic activation triggered by the emotional images.

It is important to note that our finding of enhanced memory for neutral stimuli encoded after emotional stimuli is similar to, but distinct from, prior demonstrations that emotional arousal or adrenergic agonists administered after the encoding of neutral stimuli retroactively enhances later memory for neutral information5,16,18,44,45. Post-learning arousal is proposed to heighten memory consolidation of preceding neutral information5,16,45. Here we show that pre-encoding emotional arousal that persists during exposure to neutral stimuli can prospectively influence both their initial encoding and their recollection 6 h later. Notably, BOLD activity during neutral encoding tens of minutes after emotional encoding in many respects resembled BOLD activity when participants viewed and processed emotional stimuli. Correspondingly, neutral stimuli encoded during heightened arousal showed the same mnemonic profile as emotional stimuli (enhanced recollection) relative to neutral stimuli encoded before and outside the context of emotional arousal. Taken together, these findings paint a picture of emotion as capable of biasing neutral memory via multiple mechanisms: retroactively enhancing the consolidation of previously encoded information, as well as prospectively biasing future brain states and mechanisms underlying the encoding of new experiences into memory.

Our findings that LF connectivity (amygdala–hippocampus and ventral anterior insula network correlations), subsequent recollection effects in individual brain regions (amygdala, perirhinal cortex, inferior prefrontal cortex, inferior temporal cortex) and patterns of hippocampal recollection effects characteristic of emotional encoding carried over into subsequent neutral encoding blocks are consistent with prior work showing that emotion is related to BOLD activity and connectivity in similar regions10,11,37,38,41,46,47 (assessed using a reverse analysis in neurosynth.org42). Notably, however, the present data extend these findings in several ways. First, consistent with a carry-over hypothesis, brain regions related to emotional processing and memory formation were not only engaged when participants viewed emotional stimuli but also during the subsequent encoding of neutral stimuli. This result suggests that emotion can bias BOLD activity over an extended time period (at least 9 to 33 min later). Second, differences in LF connectivity during emotional and neutral encoding in the N-E encoding order suggested that emotion modulated not only trial-by-trial evoked brain activity but also lower-frequency background BOLD activity. This modulation of background BOLD activity by emotion complements previous findings showing that background BOLD activity reflects specific types of information processing, such as distinct memory states29 and the processing of distinct stimulus classes27,28.

Although the present study found evidence that an extended emotional experience could bias future brain states and memory encoding, we note that it is unclear which specific aspects of our experimental design were critical for this effect to emerge. In our design, encoding blocks lasted for 23 min; thus, it is unclear how much time is necessary to induce a state of emotional arousal that will persist and bias future behavior. Moreover, it is also unclear how long emotional arousal may potentially last and whether this is related to the duration of the initial arousal induction. It is also noteworthy that participants performed the same task when they encountered emotional and neutral stimuli in our study (rating of visual complexity), so it is unknown whether this similarity in task context was necessary for eliciting a carry-over of an emotional state into later neutral encoding. Lastly, it is also unknown how expectations or explicit strategies developed by participants may have facilitated the reinstatement of emotional arousal or brain states during neutral encoding. Future work is needed to understand how these different factors contributed to the present findings.

The present results add to our understanding of the many ways emotion can influence memory for unrelated neutral events. When examining memories for events themselves, there is evidence that more neutral details of an emotional event may be less well remembered48,49, suggesting a trade-off in memory49,50. However, the influence of emotion on memory can also extend over time, between events. Not only can emotional arousal following a neutral event influence the storage of that event but, to the extent that arousal persists, it can also influence memory for future neutral events that are temporally and semantically distinct. Our results suggest that this prospective memory enhancement may be due to a carry-over of the brain states that underlie arousal and its influence on memory.

METHODS

Methods, including statements of data availability and any associated accession codes and references, are available in the online version of the paper.

Supplementary Material

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Note: Any Supplementary Information and Source Data files are available in the online version of the paper.

ACKNOWLEDGMENTS

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.

Footnotes

COMPETING FINANCIAL INTERESTS

The authors declare no competing financial interests.

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