Experiencing Surprise: The Temporal Dynamics of Its Impact on Memory

Abstract

To efficiently process information, the brain shifts between encoding and retrieval states, prioritizing bottom-up or top-down processing accordingly. Expectation violation before or during learning has been shown to trigger an adaptive encoding mechanism, resulting in better memory for unexpected events. Using fMRI, we explored (1) whether this encoding mechanism is also triggered during retrieval, and if so, (2) what the temporal dynamics of its mnemonic consequences are. Male and female participants studied object images, then, with new objects, they learned a contingency between a cue and a semantic category. Rule-abiding (expected) and violating (unexpected) targets and similar foils were used at test. We found interactions between previous and current similar events' expectation, such that when an expected event followed a similar but unexpected event, its performance was boosted, underpinned by activation in the hippocampus, midbrain, and occipital cortex. In contrast, a sequence of two unexpected similar events also triggered occipital engagement; however, this did not enhance memory performance. Taken together, our findings suggest that when the goal is to retrieve, encountering surprising events engages an encoding mechanism, supported by bottom-up processing, that may enhance memory for future related events.SIGNIFICANCE STATEMENT Optimizing the balance between new learning and the retrieval of existing knowledge is an ongoing process, at the core of human cognition. Previous research into memory encoding suggests experiencing surprise leads to the prioritization of the learning of new memories, forming an adaptive encoding mechanism. We examined whether this mechanism is also engaged when the current goal is to retrieve information. Our results demonstrate that an expectation-driven shift toward an encoding state, supported by enhanced perceptual processing, is beneficial for the correct identification of subsequent expected similar events. These findings have important implications for our understanding of the temporal dynamics of the adaptive encoding of information into memory.

Keywords: expectation violation; hippocampus; memory states; surprise.

Figure 1.

Experimental design. A, During the first round of encoding, participants responded whether the object was man-made or natural. In the second encoding round, participants are asked to study the object carefully. In experiment 2, each object appeared three times consecutively; in addition to the two presentations from experiment 1, participants were asked to respond whether the object was more likely to be found indoors or outdoors. The order of man-made/natural and in/outdoor questions was randomized, the third presentation was always “study carefully.” B, In the rule-learning task, participants learned a contingency between a cue and an object's category, man-made or natural. Participants had 1 s to make a decision in experiment 1, and 3 s in experiment 2. See Extended Data Figures 1-1 and 1-2 for rule-learning performance. C, In the retrieval task, the same cues were presented before each set event, old objects (targets) and new similar foils (F1, F2, F3 in experiment 1; F1 and F2 in experiment 2). On 30% of these trials, there was a mismatch between the cue and the object's category; these are unexpected trials (e.g., a cue for a natural object is followed by a man-made object, marked in red). Participants were instructed to indicate whether the object is old or new. U_prevF1, EcurrT = Unexpected F1 presented before an expected target, from the same set. D, Example of range of perceptual similarity within set events.

Figure 2.

Experiment 1 results. A, Predicting hits. More hits were observed for expected targets following unexpected F1 foils, compared with unexpected targets following unexpected F1, and compared with expected targets following expected F1. B, Predicting CR1. More CR1 for expected F1 following unexpected targets, compared with unexpected F1 following unexpected targets, and a marginal effect of poorer memory (less CR1) for a sequence of unexpected events. C, Collapsed hits and CR1. Similar results showing an interaction between the previous and current set events' expectation status, with U_prevE_curr events showing the best memory performance, compared with U_prevU_curr and E_prevE_curr. D, First set events. More hits for expected compared with unexpected targets presented first in the event sequence. No other significant effects, although F1 events follow a similar direction. Unless otherwise stated, all error bars represent 95% confidence intervals. •p = 0.0507, *p < 0.05, **p < 0.01.

Figure 3.

Behavioral and neural expectation interactions for targets and F1 foils. A, Behavioral results. Replicating the results from experiment 1, a current by previous expectation status interaction was observed, with U_prevE_curr showing a boost in memory performance. B, U_prevE_curr > E_prevE_curr contrast. Increased activation in the right hippocampus, SN/VTA, and left inferior occipital cortex. C, Unexpected > Expected interactions. Increased activation in right occipital cortex (BA 18) was observed for U_prevU_curr > E_prevE_curr, despite poor memory performance for U_prevU_curr events. D, Expected > Unexpected interactions. Increased activation in right retrosplenial cortex/precuneus for U_prevE_curr > U_prevU_curr.

Figure 4.

Overall fMRI expectation effects. A, Main effect of expectation. Unexpected events, compared with expected ones, engaged more activation in right middle occipital cortex and fusiform. Conversely, excepted events, compared with unexpected ones, engaged activation in right angular and supramarginal gyri. B, Expectation by presentation order interaction. Unexpected events presented second in the set engaged regions along the ventral visual stream. No significant effects were observed for first or third set events.

Figure 5.

Illustration of the brain networks involved in processing unexpected and expected events. Left and middle, Expectation-driven, goal-irrelevant encoding. Expectation violation engages bottom-up processing along the ventral visual stream (inferior occipital in pink, fusiform in yellow), regardless of memory performance. The subsequent mnemonic consequences of this shift toward encoding involve the hippocampus (red) and midbrain (orange) dopaminergic regions, underlying subsequent beneficial memory performance. Right, Task-driven retrieval. In the absence of expectation violation (expected events), engagement of retrieval-driven network regions to support reinstatement and memory performance, in accordance with goal to retrieve.