An official website of the United States government
Abstract Although events are not always known to be important when they occur, people can remember details about such incidentally encoded information using episodic memory. Sheridan et al. (2024) argued that rats replayed episodic memories of incidentally encoded information in an unexpected assessment of memory. In one task, rats reported the third-last item in an explicitly encoded list of trial-unique odors. In a second task, rats foraged in a radial maze in the absence of odors. On a critical test, rats foraged in the maze, but scented lids covered the food. Next, memory of the third-last odor was assessed. The rats correctly answered the unexpected question. Because the odors used in the critical test were the same as those used during training, automatically encoding odors for the purpose of taking an upcoming test of memory (stimulus generalization) may have been encouraged. Here, we provided an opportunity for incidental encoding of novel odors. Previously trained rats foraged in the radial maze with entirely novel odors covering the food. Next, memory of the third-last odor was assessed. The rats correctly answered the unexpected question. High accuracy when confronted with novel odors provides evidence that the rats did not automatically encode odors for the purpose of taking an upcoming test, ruling out stimulus generalization. We conclude that rats encode multiple pieces of putatively unimportant information, and later replayed a stream of novel episodic memories when that information was needed to solve an unexpected problem.
more »
« less
Validation of a rodent model of episodic memory replay
Vivid episodic memories in humans have been described as the replay of the flow of past events in sequential order. Recently, Panoz-Brown et al. (2018) developed an olfactory memory task in which rats were presented with a list of trial-unique odors in an encoding context; next, in a distinctive memory assessment context, the rats were rewarded for choosing the second to last item from the list while avoiding other items from the list. In a different memory assessment context, the fourth to last item was rewarded. According to the episodic memory replay hypothesis, the rat remembers the list items and searches these items to find the item at the targeted locations in the list. However, events presented sequentially differ in memory trace strength, allowing a rat to use the relative familiarity of the memory traces, instead of episodic memory replay, to solve the task. Here, we directly manipulated memory trace strength by manipulating the odor intensity of target odors in both the list presentation and memory assessment. The rats relied on episodic memory replay to solve the memory assessment in conditions in which reliance on memory trace strength is ruled out. We conclude that rats are able to replay episodic memories.
more »
« less
- Award ID(s):
- 1946039
- PAR ID:
- 10514240
- Publisher / Repository:
- Learning & Behavior
- Date Published:
- Journal Name:
- Learning & Behavior
- ISSN:
- 1543-4494
- Subject(s) / Keyword(s):
- replay episodic memory familiarity memory trace strength olfaction rat
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Context contributes to multiple aspects of human episodic memory including segmentation and retrieval. The present studies tested if, in adult male and female mice, context influences the encoding of odors encountered in a single unsupervised sampling session of the type used for the routine acquisition of episodic memories. The three paradigms used differed in complexity (single vs. multiple odor cues) and period from sampling to testing. Results show that males consistently encode odors in a context-dependent manner: the mice discriminated novel from previously sampled cues when tested in the chamber of initial cue sampling but not in a distinct yet familiar chamber. This was independent of the interval between cue encounters or the latency from initial sampling to testing. In contrast, female mice acquired both single cues and the elements of multi-cue episodes, but recall of that information was dependent upon the surrounding context only when the cues were presented serially. These results extend the list of episodic memory features expressed by rodents and also introduce a striking and unexpected sex difference in context effects.more » « less
-
null (Ed.)We show how hippocampal replay could explain latent learning, a phenomenon observed in animals where unrewarded pre-exposure to an environment, i.e. habituation, improves task learning rates once rewarded trials begin. We first describe a computational model for spatial navigation inspired by rat studies. The model exploits offline replay of trajectories previously learned by applying reinforcement learning. Then, to assess our hypothesis, the model is evaluated in a “multiple T-maze” environment where rats need to learn a path from the start of the maze to the goal. Simulation results support our hypothesis that pre-exposed or habituated rats learn the task significantly faster than non-pre-exposed rats. Results also show that this effect increases with the number of pre-exposed trials.more » « less
-
I outline the perspective that searching the contents of memory is a form of mental time travel in nonhumans that is relatively tractable because it focuses on the contents of memory. I propose that an animal model of mental time travel requires three elements: (1) the animal remembers multiple events using episodic memory, (2) the order of events in time is included in the representation, and (3) the sequence of events can be searched to find a target that occurred at a particular time. I review experiments suggesting that rats represent multiple items in episodic memory (Element 1) in order of occurrence (Element 2) and engage in memory replay to search representations in episodic memory in sequential order to find information at particular points in the sequence (Element 3). The cognitive building blocks needed for mental time travel may be quite old in the evolutionary timescale.more » « less
-
AbstractDuring spatial exploration, neural circuits in the hippocampus store memories of sequences of sensory events encountered in the environment. When sensory information is absent during ‘offline’ resting periods, brief neuronal population bursts can ‘replay’ sequences of activity that resemble bouts of sensory experience. These sequences can occur in either forward or reverse order, and can even include spatial trajectories that have not been experienced, but are consistent with the topology of the environment. The neural circuit mechanisms underlying this variable and flexible sequence generation are unknown. Here we demonstrate in a recurrent spiking network model of hippocampal area CA3 that experimental constraints on network dynamics such as population sparsity, stimulus selectivity, rhythmicity and spike rate adaptation, as well as associative synaptic connectivity, enable additional emergent properties, including variable offline memory replay. In an online stimulus‐driven state, we observed the emergence of neuronal sequences that swept from representations of past to future stimuli on the timescale of the theta rhythm. In an offline state driven only by noise, the network generated both forward and reverse neuronal sequences, and recapitulated the experimental observation that offline memory replay events tend to include salient locations like the site of a reward. These results demonstrate that biological constraints on the dynamics of recurrent neural circuits are sufficient to enable memories of sensory events stored in the strengths of synaptic connections to be flexibly read out during rest and sleep, which is thought to be important for memory consolidation and planning of future behaviour.image Key pointsA recurrent spiking network model of hippocampal area CA3 was optimized to recapitulate experimentally observed network dynamics during simulated spatial exploration.During simulated offline rest, the network exhibited the emergent property of generating flexible forward, reverse and mixed direction memory replay events.Network perturbations and analysis of model diversity and degeneracy identified associative synaptic connectivity and key features of network dynamics as important for offline sequence generation.Network simulations demonstrate that population over‐representation of salient positions like the site of reward results in biased memory replay.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- The DOI is not currently available.
