Abstract
Memory enables access to past experiences to guide future behavior. Humans can determine which memories to trust (high confidence) and which to doubt (low confidence). How memory retrieval, memory confidence, and memory-guided decisions are related, however, is not understood. In particular, how confidence in memories is used in decision making is unknown. We developed a spatial memory task in which rats were incentivized to gamble their time: betting more following a correct choice yielded greater reward. Rat behavior reflected memory confidence, with higher temporal bets following correct choices. We applied machine learning to identify a memory decision variable and built a generative model of memories evolving over time that accurately predicted both choices and confidence reports. Our results reveal in rats an ability thought to exist exclusively in primates and introduce a unified model of memory dynamics, retrieval, choice, and confidence.
Highlights
Animals rely on two sources of information to guide behavior: current sensory information from the external world and memories of the past from internal storage
We found that rats consistently bet more time on correct trials, suggestive of a memory confidence computation
The task allowed us to address the long-standing challenge of defining a memory decision variable (MDV): we trained a deep neural network (DNN) on an exhaustive list of task observables to predict choice accuracy and interpreted its output detection statistic as defining a synthetic memory difficulty axis or decision variable, the MDVDNN
Summary
Animals rely on two sources of information to guide behavior: current sensory information from the external world and memories of the past from internal storage. Because sensory perception and memory are both imperfect, metacognitive monitoring of their possible errors can valuably inform future action, for instance, by motivating information seeking prior to decisions or decreased resource investment afterward.[1,2,3,4,5,6] Studies of this metacognitive monitoring have focused primarily on confidence in information perceived externally (e.g., motion detection and odor discrimination), reporting confidence-related behaviors across multiple species, including dolphins,[7] non-human primates,[8,9,10,11,12] honeybees,[13] and rats.[14,15] A statistical framework that formally defines confidence and its signatures[14,16,17] has helped establish a correspondence between statistical confidence in perceptions and the subjective sense of human confidence[18] and enabled the identification of behavioral and neural confidence markers in species including macaques,[10,19] pre-verbal infants,[20] and rats.[21,22]. We lack a quantitative account of how memories evolve over time, and we do not understand how this evolution could lead to behavioral expressions of confidence
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