Surprise and destabilize: prediction error influences episodic memory reconsolidation

Abstract

Through the process of "reconsolidation," reminders can temporarily destabilize memories and render them vulnerable to change. Recent rodent research has proposed that prediction error, or the element of surprise, is a key component of this process; yet, this hypothesis has never before been extended to complex episodic memories in humans. In our novel paradigm, we used naturalistic stimuli to demonstrate that prediction error enables adaptive updating of episodic memories. In Study 1, participants ( = 48) viewed 18 videos, each depicting an action-outcome event. The next day, we reactivated these memories by presenting the videos again. We found that incomplete reminders, which interrupted videos before the outcome, made memories vulnerable to subsequent interference from a new set of videos, producing false memories. In Study 2 ( = 408), an independent sample rated qualities of the stimuli. We found that videos that were more surprising when interrupted produced more false memories. Last, in Study 3 ( = 24), we tested competing predictions of reconsolidation theory and the Temporal Context Model, an alternative account of source confusion. Consistent with the mechanistic time-course of reconsolidation, our effects were crucially time-dependent. Overall, we synthesize prior animal and human research to present compelling evidence that prediction error destabilizes episodic memories and drives dynamic updating in the face of new information.

Prediction errors indexed by the P3 track the updating of complex long-term memory schemas

“…Here, larger PEs were associated with a relative decrease in responding with locations that were consistent with the old schema, apparent in reduced evidence of responses -90 degrees from the current schema (i.e., at the position of the old schema for the inconsistent conditions) compared to what was observed in the consistent conditions. My work reveals that similar neural mechanisms underlie PE-based updating of long-term memory schemas, and short-term beliefs (Bennett et al, 2015;Jepma et al, 2018Jepma et al, , 2016Kolossa et al, 2015), consistent with what has been proposed in the literature (van Kesteren et al, 2012), and what has been shown for other types of memory (Greve et al, 2017(Greve et al, , 2019Pine et al, 2018;Sinclair & Barense, 2018.…”

“…Henson & Gagnepain, 2010;van Kesteren, Ruiter, Fernández, & Henson, 2012): When a predicted outcome does not match our experience, the resulting PE provides us with a surprise signal that is believed to guide learning. Recent findings suggest that PEbased learning underlies memory updating in many contexts: the updating of schematic rules (Greve, Cooper, Tibon, & Henson, 2019), of episodic memories (Greve, Cooper, Kaula, Anderson, & Henson, 2017;Sinclair & Barense, 2018, and of single semantic facts (Pine, Sadeh, Ben-Yakov, Dudai, & Mendelsohn, 2018).…”

Reward Prediction Error and Declarative Memory

“…This finding is most intensively studied in non-declarative memory [60], but is observed in declarative memory as well [61]. PE is required for reconsolidation [62] both in non-declarative [63] and in declarative memory [61,64]. Given the important role of RPE in declarative learning, and given that similar principles drive learning and reconsolidation [64], we predict that RPE may modulate reconsolidation too.…”

“…When information is retrieved from memory, it enters a plastic, labile state, allowing the information to be changed, strengthened or weakened, a process called reconsolidation [58,59]. This finding is most intensively studied in non-declarative memory [60], but is observed in declarative memory as well [61]. PE is required for reconsolidation [62] both in non-declarative [63] and in declarative memory [61,64].…”

Behavioral, physiological, and neural signatures of surprise during naturalistic sports viewing

“…Of course, our predictions are not always correct -when they are inaccurate, we experience surprise (i.e., unsigned prediction error [1][2][3][4][5]. Surprise is theorized to be critical for learning and memory 6,7 , updating our beliefs about the structure of the world 8 , and demarcating events in the continuous flow of time 9 . Moreover, although people typically prefer certainty about outcomes that are instrumental for survival 10 , in domains with noninstrumental information, such as narratives, music, and sports, people tend to prefer violations of their expectations [11][12][13] , suggesting that surprise is often a rewarding affective experience.…”