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Prior research has used innovative paradigms to show that some non-human animal species demonstrate behavioural choices (i.e. foraging for a food item at a specific location, and at a time that guarantees it has not yet decayed), reflecting episodic-like or 'WWW' memory (memory for 'what' happened, 'where' and 'when'). These results raised the question of whether similar approaches could be used to examine memory in young children in order to reduce verbal demands. The present research examines the extent to which children's WWW memory aligns with memory-based choices in 3- to 5-year-olds (n = 95; study 1) and in 7- to 11-year-olds and adults (n = 168; study 2). Results indicate that preschoolers' struggle with choice-based tasks probably reflects difficulty integrating their WWW memory with an understanding that certain items decay over time. Moreover, a convergence between verbal recall measures and choice-based measures is observable in 7-year-olds and beyond, reflecting a stronger integration of memory signals, understanding of state transformation, and decision-making. This article is part of the theme issue 'Elements of episodic memory: lessons from 40 years of research'.

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I outline the perspective that searching the contents of memory is a form of mental time travel (MTT) in non-humans that is relatively tractable because it focuses on the contents of memory. I propose that an animal model of MTT requires three elements: (i) the animal remembers multiple events using episodic memory, (ii) the order of events in time is included in the representation, and (iii) 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 MTT may be quite old in the evolutionary timescale.This article is part of the theme issue 'Elements of episodic memory: lessons from 40 years of research'.

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Episodic memory and mental time travel have been viewed as uniquely human traits.1,2,3 This view began to shift with the development of behavioral criteria to assess what is referred to as "episodic-like memory" in animals.4,5 Key findings have ranged from evidence of what-where-when memory in scrub-jays, rats, and bees; through decision-making that impacts future foraging in frugivorous primates; to evidence of planning based on future needs in scrub-jays and tool use planning in great apes.4,6,7,8,9,10,11,12,13 Field studies of these issues have been rare, though there is field-based evidence for future-oriented behaviors in primates.8,10,14,15 We report evidence that free-ranging wild fruit bats rely on mental temporal maps and exhibit future-oriented behaviors when foraging. We tracked young bats as they navigated and foraged, documenting every tree they visited over many months. We prevented the bats from foraging outside for different time periods and monitored their foraging decisions, revealing that the bats map the spatiotemporal patterns of resources in their environment. Following a long period in captivity, the bats did not visit those trees that were no longer providing fruit. We show that this time-mapping ability requires experience and is lacking in inexperienced bats. Careful analysis of the bats' movement and foraging choices indicated that they plan which tree to visit while still in the colony, thus exhibiting future-oriented behavior and delayed gratification on a nightly basis. Our findings demonstrate how the need for spatiotemporal mental mapping can drive the evolution of high cognitive abilities that were previously considered exclusive to humans.

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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.

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Although events are not always known to be important when they occur, people can remember details about such incidentally encoded information using episodic memory. Importantly, when information is explicitly encoded for use in an expected test of retention (as in most assessments in animals), it is possible that it is used to generate a planned action1,2,3; thus, the remembered action can occur without remembering the earlier episode. By contrast, when a test is unexpected, transforming information into an action plan is unlikely because the importance of the information and the nature of the test are not yet known. Thus, accurate performance in an unexpected test after incidental encoding documents episodic memory.1,2,3,4,5,6,7,8 Here, we present evidence that rats replay episodic memories of incidentally encoded information in an unexpected assessment of memory. In one task,9 rats reported the third-last item in an explicitly encoded list of trial-unique odors. In a second task,10 rats foraged in a radial maze in the absence of odors. On a critical test, rats foraged in the radial maze, but scented lids covered the food. Next, memory of the third-last odor was assessed. All participating rats correctly answered the unexpected question. These results suggest that rats encoded multiple pieces of putatively unimportant information, and later they replayed a stream of episodic memories when that information was needed to solve an unexpected problem. We propose that rats replay episodic memories of incidentally encoded information, which documents a critical aspect of human episodic memory in a non-human animal.

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Scatter-hoarding birds find their caches using spatial memory and have an enlarged hippocampus. Finding a cache site could be achieved using either Recollection (a discrete recalling of previously experienced information) or Familiarity (a feeling of "having encountered something before"). In humans, these two processes can be distinguished using receiver operating characteristic (ROC) curves. ROC curves for olfactory memory in rats have shown the hippocampus is involved in Recollection, but not Familiarity. We test the hypothesis that food-hoarding birds, having a larger hippocampus, primarily use Recollection to find their caches. We validate a novel method of constructing ROC curves in humans and apply this method to cache retrieval by coal tits (Periparus ater). Both humans and birds mainly use Familiarity in finding their caches, with lower contribution of Recollection. This contribution is not significantly different from chance in birds, but a small contribution cannot be ruled out. Memory performance decreases with increasing retention interval in birds. The ecology of food-hoarding Parids makes it plausible that they mainly use Familiarity in the memory for caches. The larger hippocampus could be related to associating cache contents and temporal context with cache locations, rather than Recollection of the spatial information itself.

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Episodic-like memory (ELM) consists in the capacity of nonhuman animals to remember 'where' and 'when' a specific episode occurred ('what'). Previous studies have showed that Wistar rats can form an ELM, but not after a 24 h retention delay. On the other hand, it has been demonstrated that caffeine can improve episodic memory consolidation in humans. Therefore, we verified whether acute post-sample caffeine administration could improve ELM consolidation in Wistar rats, as well if it could be related to neurochemical changes in the prefrontal cortex and hippocampus - regions related to episodic-like memory processing. 46 Male Wistar Rats, approximately 3 months-old, were divided into four groups as follows: untreated (n = 11), saline (n = 11), caffeine 10 mg ∕kg i.p (n = 12); caffeine 15 mg∕kgi.p (n = 12) and tested in WWWhen/ELM task. The animals treated with caffeine in different dosages (10 mg/kg and 15 mg/kg) discriminated temporally and spatially the objects, respectively. These groups also showed a dopamine renewal rate in the hippocampus, suggesting that there was an increase in the turnover compared with the groups with no caffeine administration. We can conclude that caffeine leads to an improvement in the consolidation of the temporal ('what-when') and spatial ('what-where') aspects of episodic-like memory.

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Cortical oscillations in different frequency bands have been shown to be intimately involved in exploration of environment and cognition. Here, the local field potentials in the hippocampus, the medial prefrontal cortex (mPFC), and the medial entorhinal cortex (mEC) were recorded simultaneously in rats during the execution of the episodic-like memory task. The power of theta (~4-10 Hz), slow gamma (~25-50 Hz), and fast gamma oscillations (~55-100 Hz) was analyzed in all structures examined. Particular attention was paid to the theta coherence between three mentioned structures. The modulation of the power of gamma rhythms by the phase of theta cycle during the execution of the episodic-like memory test by rats was also closely studied. Healthy rats and rats one month after kainate-induced status epilepticus (SE) were examined. Paroxysmal activity in the hippocampus (high amplitude interictal spikes), excessive excitability of animals, and the death of hippocampal and dentate granular cells in rats with kainate-evoked SE were observed, which indicated the development of seizure focus in the hippocampus (epileptogenesis). One month after SE, the rats exhibited a specific impairment of episodic memory for the what-where-when triad: unlike healthy rats, epileptogenic SE animals did not identify the objects during the test. This impairment was associated with the changes in the characteristics of theta and gamma rhythms and specific violation of theta coherence and theta/gamma coupling in these structures in comparison with the healthy animals. We believe that these disturbances in the cortical areas play a role in episodic memory dysfunction in kainate-treated animals. These findings can shed light on the mechanisms of cognitive deficit during epileptogenesis.

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AIMS: Entorhinal cortex (EC) deep brain stimulation (DBS) has shown a memory enhancement effect. However, its brain network modulation mechanisms remain unclear. The present study aimed to investigate the functional connectivity in the rat hippocampal-cortex network and episodic-like memory performance following EC-DBS. METHODS: 7.0 T functional MRI (fMRI) scans and episodic-like memory tests were performed 3 days and 28 days after EC-DBS in healthy rats. The fMRI data processing was focused on the power spectra, functional connectivity, and causality relationships in the hippocampal-cortex network. In addition, the exploration ratio for each object and the discrimination ratio of the "when" and "where" factors were calculated in the behavioral tests. RESULTS: EC-DBS increased the power spectra and the functional connectivity in the prefrontal- and hippocampal-related networks 3 days after stimulation and recovered 4 weeks later. Both networks exhibited a strengthened connection with the EC after EC-DBS. Further seed-based functional connectivity comparisons showed increased connectivity among the prefrontal cortex, hippocampus and EC, especially on the ipsilateral side of DBS. The dentate gyrus is a hub region closely related to both the EC and the prefrontal cortex and receives information flow from both. Moreover, acute EC-DBS also enhanced the discrimination ratio of the "where" factor in the episodic-like memory test on Day 3. CONCLUSION: EC-DBS caused a reversible modulation effect on functional connectivity in the hippocampal-cortex network and episodic-like memory performance.

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Yellow warblers (Setophaga petechia) use referential 'seet' calls to warn mates of brood parasitic brown-headed cowbirds (Molothrus ater). In response to seet calls during the day, female warblers swiftly move to sit tightly on their nests, which may prevent parasitism by physically blocking female cowbirds from inspecting and laying in the nest. However, cowbirds lay their eggs just prior to sunrise, not during daytime. We experimentally tested whether female warblers, warned by seet calls on one day, extend their anti-parasitic responses into the future by engaging in vigilance at sunrise on the next day, when parasitism may occur. As predicted, daytime seet call playbacks caused female warblers to leave their nests less often on the following morning, relative to playbacks of both their generic anti-predator calls and silent controls. Thus, referential calls do not only convey the identity or the type of threat at present but also elicit vigilance in the future to provide protection from threats during periods of heightened vulnerability.

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Place memory, the ability to remember locations, is a feature of many animal species. This episodic-like memory is displayed in the foraging behavior of animals and has been studied in many different kinds of laboratory spatial tasks. A horse stallion, Equus ferus caballus, will create "dung-heaps or stud-piles" by defecation in the same place suggesting that the behavior is central to spatial behavior but to date there has been little investigation of horse olfactory/spatial behavior. The present study describes investigatory behavior of horses for objects on the surface of a riding arena. Horses under saddle approached objects on the arena surface that included small pieces of straw, fur, and paper and larger objects including clumps of debris and were especially interested in dung droppings left by other horses. Once an object was investigated by sniffing, it was usually not approached again during that outing but could be approached anew on the following day. Dung investigatory behavior and place memory were confirmed in a number of structured tests in which test-retest intervals were varied. The results are discussed in relation to the dual process theory that proposes that spatial representations central to adaptive behavior require both allocentric Cartesian spatial information and egocentric episodic-like information.

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Workers of the ant Myrmica sabuleti have been previously shown to be able to add and subtract numbers of elements and to expect the time and location of the next food delivery. We wanted to know if they could anticipate the following quantity of elements present near their food when the number of these elements increases or decreases over time according to an arithmetic sequence. Two experiments were therefore carried out, one with an increasing sequence, the other with a decreasing sequence. Each experiment consisted of two steps, one for the ants to learn the numbers of elements successively present near their food, the other to test their choice when they were simultaneously in the presence of the numbers from a previously learned sequence and the following quantity. The ants anticipated the following quantity in each presented numerical sequence. This forethinking of the next quantity applies to numerosity, thus, to concrete items. This anticipatory behavior may be explained by associative learning and by the ants' ability to memorize events and to estimate the elapsing time.

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BACKGROUND: Episodic-like memory tasks based on the spontaneous exploration of objects are commonly applied in one-trial protocols. However, multiple-trial designs are known to reduce animal numbers and data variance, providing faster accumulation of data. NEW METHOD: In this study, we devised a new object recognition memory task for rats that carry out multiple trials per session. We developed three types of continual trial tasks: a longer protocol, a shorter protocol, and a protocol in which the experimental session was divided into two days. RESULTS: In our design, rats expressed temporal and spatial memory, but not what-where-when content integration. We found that shorter protocols were more efficient to evaluate memory capabilities. COMPARISON WITH EXISTING METHODS: To the best of our knowledge, it is the first object recognition task with multiple trials that simultaneously assess the temporal and spatial aspects of episodic-like memory. CONCLUSIONS: We suggest that our task is suitable for the simultaneous measurements of brain functions related to spatial and temporal attributes in rats.

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Episodic memory refers to the recollection of previous experiences containing specific temporal, spatial, and emotional information. The ability to recollect episodic memory requires coordination of multiple brain regions, including the hippocampus (HPC) and the cingulate cortex. While the afferents into HPC and cingulate cortex that orchestrate the episodic memory remain unclear. The medial septum (MS), one of the anatomical location of cholinergic centers, innervates not only the dorsal HPC (dHPC), but also the cingulate and entorhinal cortices. By using "What-Where-When" episodic-like memory (ELM) behavioral model and viral tracing, we found that MS neurons projected to dHPC and anterior cingulate cortex (ACC), which exerted distinct impacts on ELM recollection. Chemogenetic inhibition of the dHPC-projecting MS neurons disrupted "What-Where-When" ELM recollection as well as object location, object-in-place, and recency recognition memories recollection, while chemogenetic inhibition of the ACC-projecting MS neurons only disrupted "What-Where-When" ELM recollection. Moreover, neither dHPC- nor ACC-projecting MS neurons were involved in novel object recognition memory recollection or locomotor activity. Immunostaining showed that ACC- and dHPC-projecting MS neurons are partially overlapped populations. These findings reveal an unsuspected division of ELM processing and provide the potential mechanism that the recollection of episodic memory need the coordination of MS neurons projecting to dHPC and ACC.

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Definitions of episodic memory typically emphasise the importance of spatiotemporal frameworks in the contextual reconstruction of episodic retrieval. However, our ability to retrieve specific temporal contexts of experienced episodes is poor. This has bearing on the prominence of temporal context in the definition and evaluation of episodic memory, particularly among non-human animals. Studies demonstrating that rats rely on elapsed time (distance) rather than specific timestamps (location) to disambiguate events have been used to suggest that human episodic memory is qualitatively different to other species. We examined whether humans were more accurate using a distance- or location-based method for judging when an event happened. Participants (n = 57) were exposed to a series of events and then asked either when (e.g., 1:03 pm) or how long ago (HLA; e.g., 33 min) a specific event took place. HLA judgements were significantly more accurate, particularly for the most recently experienced episode. Additionally, a significantly higher proportion of participants making HLA judgements accurately recalled non-temporal episodic features across all episodes. Finally, for participants given the choice of methods for making temporal judgements, a significantly higher proportion chose to use HLA judgements. These findings suggest that human and non-human temporal judgements are not qualitatively different.

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To investigate the effects of retrosplenial cortex (RSC) lesions on episodic-like memory, we used four types of object recognition tasks. What task examined memory of object identities. Where task examined memory of object locations. When task examined memory of the temporal order of presented objects. Episodic task examined the integrated memory of the identity, location, and temporal order of presented objects. Rats with the RSC lesions preferred novel objects in the What and Where tasks, whereas they showed no such preference in the When and Episodic tasks, suggesting that rats with the RSC lesions have deficits in memory for temporal order and that this might cause deficits in episodic-like memory.

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A number of studies have provided evidence that animals, including rats, remember past episodes. However, few experiments have addressed episodic-like memory from a social perspective. In the present study, we evaluated Wistar rats in the WWWhen/ELM task as single setups and in dyads, applying a long retention interval. We also investigated behaviors that could subserve the emergence of this type of memory. We found that only rats tested in the social setting were able to recollect an integrated episodic-like memory that lasted 24 h. Additionally, rats in dyads presented higher levels of exploration during the task. When exposed to the testing environment, the dyads exhibited affiliative behavior toward each other and presented fewer anxiety-like responses. Our findings indicate that the presence of a conspecific could act as a facilitating factor in memory evaluations based on spontaneous exploration of objects and provide empirical support for applying more naturalistic settings in investigations of episodic-like memory in rats.

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Humans spend the lion's share of their mental life either in their personal past or an anticipated or imagined future. This type of mental state is known as mental time travel. It is perhaps the most sophisticated and fitness-promoting cognition that has evolved in humans and with some reservation in animals. We have proposed that working memory capacity and the complexity of executive functions within working memory might limit the authenticity with which past events are reconstructed and anticipated or imagined future scenarios are constructed. In the present article, we discuss the possibility of a co-evolution between working memory capacity, complexity of executive functions available in the working memory workspace, and mental time travel abilities across species. We further assume that a complex working memory system can be constructed with quite different brains and conclude that the advanced cognitive function of thinking about the past and the future might not be a privilege of the mammalian brain.

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Down syndrome (DS), a genetic disorder caused by partial or complete triplication of chromosome 21, is the most common genetic cause of intellectual disability. DS mouse models and cell lines display defects in cellular adaptive stress responses including autophagy, unfolded protein response, and mitochondrial bioenergetics. We tested the ability of hydroxyurea (HU), an FDA-approved pharmacological agent that activates adaptive cellular stress response pathways, to improve the cognitive function of Ts65Dn mice. The chronic HU treatment started at a stage when early mild cognitive deficits are present in this model (∼3 months of age) and continued until a stage of advanced cognitive deficits in untreated mice (∼5-6 months of age). The HU effects on cognitive performance were analyzed using a battery of water maze tasks designed to detect changes in different types of memory with sensitivity wide enough to detect deficits as well as improvements in spatial memory. The most common characteristic of cognitive deficits observed in trisomic mice at 5-6 months of age was their inability to rapidly acquire new information for long-term storage, a feature akin to episodic-like memory. On the background of severe cognitive impairments in untreated trisomic mice, HU-treatment produced mild but significant benefits in Ts65Dn by improving memory acquisition and short-term retention of spatial information. In control mice, HU treatment facilitated memory retention in constant (reference memory) as well as time-variant conditions (episodic-like memory) implicating a robust nootropic effect. This was the first proof-of-concept study of HU treatment in a DS model, and indicates that further studies are warranted to assess a window to optimize timing and dosage of the treatment in this pre-clinical phase. Findings of this study indicate that HU has potential for improving memory retention and cognitive flexibility that can be harnessed for the amelioration of cognitive deficits in normal aging and in cognitive decline (dementia) related to DS and other neurodegenerative diseases.

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Episodic-like memory refers to integration of where and when a certain event (what) happened. The glutamatergic neurotransmission, particularly AMPA and NMDA receptors, in the dorsal hippocampus mediates episodic recall. Ketamine is a non-competitive NMDA antagonist with effect on cognitive performance and plasticity. The goal of this study was to evaluate the acute action of ketamine on behavioural and neurochemical aspects of episodic-like memory (WWWhen/ELM task) through immediate-early gene expression (IEG), c-Fos, in the dorsal hippocampus. Animals received saline 0.9% or ketamine at 8 mg/kg or 15 mg/kg (i.p.) immediately after the second sample. Our data indicate that untreated and saline rats integrate the three elements of episodic-like memory. Conversely, animals treated with ketamine showed impairment of ELM formation. In addition, the highest dose of ketamine increased c-Fos expression in dorsal CA1 subregion when compared to saline rats. Our results indicate that the antagonism of NMDA concurrently impair ELM formation of all three aspects of ELM and increase neuronal activation in dorsal CA1.

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