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1. Offline memory replay in recurrent neuronal networks emerges from constraints on online dynamics

   https://doi.org/10.1113/JP283216  

   Milstein, Aaron D. ; Tran, Sarah ; Ng, Grace ; Soltesz, Ivan ( August 2023 , The Journal of Physiology)

   During 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

   A 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.

    

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2. Reductions in Retrieval Competition Predict the Benefit of Repeated Testing

   https://doi.org/10.1038/s41598-018-29686-y  

   Rafidi, Nicole S. ; Hulbert, Justin C. ; Brooks, Paula P. ; Norman, Kenneth A. ( August 2018 , Scientific Reports)

   Repeated testing leads to improved long-term memory retention compared to repeated study, but the mechanism underlying this improvement remains controversial. In this work, we test the hypothesis that retrieval practice benefits subsequent recall by reducing competition from related memories. This hypothesis implies that the degree of reduction in competition between retrieval practice attempts should predict subsequent memory for practiced items. To test this prediction, we collected electroencephalography (EEG) data across two sessions. In the first session, participants practiced selectively retrieving exemplars from superordinate semantic categories (high competition), as well as retrieving the names of the superordinate categories from exemplars (low competition). In the second session, participants repeatedly studied and were tested on Swahili-English vocabulary. One week after session two, participants were again tested on the vocabulary. We trained a within-subject classifier on the data from session one to distinguish high and low competition states. We then used this classifier to measure the change in competition across multiple successful retrieval practice attempts in the second session. The degree to which competition decreased for a given vocabulary word predicted whether it was subsequently remembered in the third session. These results are consistent with the hypothesis that repeated testing improves retention by reducing competition.

    

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3. Visual short‐term memory for high resolution associations is impaired in patients with medial temporal lobe damage

   https://doi.org/10.1002/hipo.22682  

   Koen, Joshua D. ; Borders, Alyssa A. ; Petzold, Michael T. ; Yonelinas, Andrew P. ( December 2016 , Hippocampus)

   The medial temporal lobe (MTL) plays a critical role in episodic long‐term memory, but whether the MTL is necessary for visual short‐term memory is controversial. Some studies have indicated that MTL damage disrupts visual short‐term memory performance whereas other studies have failed to find such evidence. To account for these mixed results, it has been proposed that the hippocampus is critical in supporting short‐term memory for high resolution complex bindings, while the cortex is sufficient to support simple, low resolution bindings. This hypothesis was tested in the current study by assessing visual short‐term memory in patients with damage to the MTL and controls for high resolution and low resolution object‐location and object‐color associations. In the location tests, participants encoded sets of two or four objects in different locations on the screen. After each set, participants performed a two‐alternative forced‐choice task in which they were required to discriminate the object in the target location from the object in a high or low resolution lure location (i.e., the object locations were very close or far away from the target location, respectively). Similarly, in the color tests, participants were presented with sets of two or four objects in a different color and, after each set, were required to discriminate the object in the target color from the object in a high or low resolution lure color (i.e., the lure color was very similar or very different, respectively, to the studied color). The patients were significantly impaired in visual short‐term memory, but importantly, they were more impaired for high resolution object‐location and object‐color bindings. The results are consistent with the proposal that the hippocampus plays a critical role in forming and maintaining complex, high resolution bindings. © 2016 Wiley Periodicals, Inc.

    

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4. ‘Sleep-dependent’ memory consolidation? Brief periods of post-training rest and sleep provide an equivalent benefit for both declarative and procedural memory

   https://doi.org/10.1101/lm.053330.120  

   Wang, Serene Y. ; Baker, Kirsten C. ; Culbreth, Jessica L. ; Tracy, Olivia ; Arora, Madison ; Liu, Tingtong ; Morris, Sydney ; Collins, Megan B. ; Wamsley, Erin J. ( May 2021 , Learning & Memory)

   Sleep following learning facilitates the consolidation of memories. This effect has often been attributed to sleep-specific factors, such as the presence of sleep spindles or slow waves in the electroencephalogram (EEG). However, recent studies suggest that simply resting quietly while awake could confer a similar memory benefit. In the current study, we examined the effects of sleep, quiet rest, and active wakefulness on the consolidation of declarative and procedural memory. We hypothesized that sleep and eyes-closed quiet rest would both benefit memory compared with a period of active wakefulness. After completing a declarative and a procedural memory task, participants began a 30-min retention period with PSG (polysomnographic) monitoring, in which they either slept ( n = 24), quietly rested with their eyes closed ( n = 22), or completed a distractor task ( n = 29). Following the retention period, participants were again tested on their memory for the two learning tasks. As hypothesized, sleep and quiet rest both led to better performance on the declarative and procedural memory tasks than did the distractor task. Moreover, the performance advantages conferred by rest were indistinguishable from those of sleep. These data suggest that neurobiology specific to sleep might not be necessary to induce the consolidation of memory, at least across very short retention intervals. Instead, offline memory consolidation may function opportunistically, occurring during either sleep or stimulus-free rest, provided a favorable neurobiological milieu and sufficient reduction of new encoding. 

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5. Cognitive tasks affect the relationship between representational pattern similarity and subsequent item memory in the hippocampus

   https://doi.org/10.1016/j.neuroimage.2023.120241  

   Lim, Ye-Lim ; Lang, Davis J. ; Diana, Rachel A. ( August 2023 , NeuroImage)

   Episodic memories are records of personally experienced events, coded neurally via the hippocampus and sur- rounding medial temporal lobe cortex. Information about the neural signal corresponding to a memory representation can be measured in fMRI data when the pattern across voxels is examined. Prior studies have found that similarity in the voxel patterns across repetition of a to-be-remembered stimulus predicts later memory retrieval, but the results are inconsistent across studies. The current study investigates the possibility that cognitive goals (defined here via the task instructions given to participants) during encoding affect the voxel pattern that will later support memory retrieval, and therefore that neural representations cannot be interpreted based on the stimulus alone. The behavioral results showed that exposure to variable cognitive tasks across repetition of events benefited subsequent memory retrieval. Voxel patterns in the hippocampus indicated a significant interaction between cognitive tasks (variable vs. consistent) and memory (remembered vs. forgotten) such that reduced voxel pattern similarity for repeated events with variable cognitive tasks, but not consistent cognitive tasks, sup- ported later memory success. There was no significant interaction in neural pattern similarity between cognitive tasks and memory success in medial temporal cortices or lateral occipital cortex. Instead, higher similarity in voxel patterns in right medial temporal cortices was associated with later memory retrieval, regardless of cognitive task. In conclusion, we found that the relationship between pattern similarity across repeated encoding and memory success in the hippocampus (but not medial temporal lobe cortex) changes when the cognitive task during encoding does or does not vary across repetitions of the event. 

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