The neural correlates of different sources of surprise: Evidence from two naturalistic fMRI studies
Presented During:
Wednesday, June 26, 2024: 11:30 AM - 12:45 PM
COEX
Room:
ASEM Ballroom 202
Poster No:
1071
Submission Type:
Abstract Submission
Authors:
Dominika Varga1, Petar Raykov2, Elizabeth Jefferies3, Aya Ben-Yakov4, Chris Bird1
Institutions:
1University of Sussex, Brighton, United Kingdom, 2MRC CBU, Cambridge, United Kingdom, 3University of York, York, United Kingdom, 4The Edmond and Lily Safra Center for Brain Sciences (ELSC), Jerusalem, Israel
First Author:
Co-Author(s):
Introduction:
In general, we experience surprise when an observation contradicts expectations based on our past experiences. However, we can be surprised for different reasons, depending on the source of our expectations. Expectations can be flexibly drawn from either our general knowledge about how the world works or memories of specific episodes in the past. Because current leading theories on how surprising events are processed do not account for this complexity in sources of predictions, it is unclear if surprise based on different sources of expectations engage the same or distinct neural processes. A currently prominent view is that the hippocampus acts as a comparator between prior experience and incoming information, and plays an important role in detecting events that mismatch our expectations (e.g. Kumaran & Maguire, 2007; Barron, Auksztulewicz, Friston, 2020). However, this idea stems from work in which participants learned arbitrary associations which were violated after minimal delay. For example, violating the temporal order or spatial arrangement of recently experienced items (e.g. Kumaran & Maguire, 2006; Duncan et al., 2012). In short, these studies have demonstrated a role of the hippocampus in processing surprise based on episodic-like memories. However, outside of the laboratory we often rely on our general semantic or schematic knowledge to predict what is likely to happen in a given situation (Elman & McRae, 2019). While some theories predict increased hippocampal engagement when there is a mismatch between prior schematic knowledge and current experience (e.g. SLIMM framework, van Kesteren et al., 2012), there is no direct evidence to support this idea.
Methods:
Across two fMRI experiments (Experiment 1 N=36; Experiment 2 N=33; Fig. 1), we tested the hippocampus' role in processing unexpected events based on general knowledge or episodic memory-based predictions. We created 34 pairs of custom made video clips that showed actors carrying out sequences of actions in a range of everyday situations. Each pair of clip included an Unexpected version, where the actor carried out an unexpected sequence of actions (e.g., putting flowers into a washing machine), and a corresponding Expected version, where the unexpected action was replaced by an expected, context-congruent action (e.g., putting clothes into a washing machine). In both experiments we showed 17 Unexpected and 17 Expected clips in the scanner. Crucially, we manipulated participants' pre-scan exposure to the clips, either having no pre-exposure and only showing clips inside the scanner (Expt 1), or showing all clips in the Expected version before scanning (Expt 2). This meant that Experiment 1 participants could be surprised only based on their general knowledge of everyday situations, while Experiment 2 participants could also be surprised based on their memory for the specific clips.
·Figure 1. Stimuli (Top) and Experimental Design (Bottom)
Results:
A significant action-expectedness by prediction-source interaction showed that hippocampal univariate activity increased to Unexpected relative to Expected actions when predictions relied on memory for specific clips (Expt 2), but not when predictions relied on general knowledge (Expt 1), suggesting that this region does not have a general role in processing unexpected events. Exploratory network analyses showed increased response to Unexpected actions in the Semantic Control and Multiple Demand Network in both experiments, suggesting that these networks have a role in processing information incongruent with the general context. Conversely, activity in the Default Mode Network increased to Unexpected actions only in Experiment 2, suggesting that this network is involved when input violates internally stored representations of specific contexts. See Fig. 2.
·Figure 2. fMRI Results. The effect of prediction source on hippocampal (Top) and networkwide (Bottom) response to expected and unexpected actions.
Conclusions:
We show that differentiating expectation sources is crucial in studying neural responses to surprise. Our results contradict a general role for the hippocampus in processing unexpected events, informing updates to models of mismatch detection.
Learning and Memory:
Long-Term Memory (Episodic and Semantic) 1
Modeling and Analysis Methods:
Activation (eg. BOLD task-fMRI) 2
Univariate Modeling
Keywords:
Cognition
Experimental Design
FUNCTIONAL MRI
Memory
NORMAL HUMAN
Pre-registration
Univariate
Other - Prediction
1|2Indicates the priority used for review
Provide references using author date format
Duncan, K. et al. (2012). Evidence for area CA1 as a match/mismatch detector: a highâresolution fMRI study of the human hippocampus. Hippocampus, vol. 22, no. 3, pp.389-398.
Elman, J.L. et al. (2019). A model of event knowledge. Psychological Review, vol. 126, no. 2, p.252.
Kumaran, D. et al. (2007). Which computational mechanisms operate in the hippocampus during novelty detection?. Hippocampus, vol. 17, no. 9, pp.735-748.
Kumaran, D. et al. (2006_. An unexpected sequence of events: mismatch detection in the human hippocampus. PLoS biology, vol. 4, no. 12, p.e424.
Van Kesteren, M.T. et al. (2012). How schema and novelty augment memory formation. Trends in neurosciences, vol. 35, no. 4, pp.211-219.