Neural systems underlying episodic memory: insights from animal research.

Early cognitive neuroscientific research revealed that the hippocampus is crucial for spatial navigation in rodents, and for autobiographical episodic memory in humans. Researchers quickly linked these streams to propose that the human hippocampus supports memory through its role in representing space, and research on the link between spatial cognition and episodic memory in humans has proliferated over the past several decades. Different researchers apply the term "spatial" in a variety of contexts, however, and it remains unclear what aspect of space may be critical to memory. Similarly, "episodic" has been defined and tested in different ways. Naturalistic assessment of spatial memory and episodic memory (i.e., episodic autobiographical memory) is required to unify the scale and biological relevance in comparisons of spatial and mnemonic processing. Limitations regarding the translation of rodent to human research, human ontogeny, and inter-individual variability require greater consideration in the interpretation of this literature. In this review, we outline the aspects of space that are (and are not) commonly linked to episodic memory, and then we discuss these dimensions through the lens of individual differences in naturalistic autobiographical memory. Future studies should carefully consider which aspect(s) of space are being linked to memory within the context of naturalistic human cognition. This article is categorized under: Psychology > Memory.

Progress on the hippocampal circuits and functions based on sharp wave ripples

What-Where-When (WWW) memory tasks have been used to study episodic(-like) memory in non-human animals. In this study, we investigate whether humans use episodic memory to solve such a WWW memory task. Participants are assigned to one of two treatments, in which they hide different coin types (what) in different locations (where) on two separate occasions (when). In the Active treatment, which mimics the animal situation as closely as possible, participants are instructed to memorize the WWW information; in the Passive treatment, participants are unaware of the fact that memory will be tested. In both groups, the majority of participants report using a mental time travel strategy to solve the task, and performance on a different episodic memory test significantly predicts performance on the WWW memory task. This suggests that the WWW memory task is a good test of episodic memory in humans. Participants remember locations and coins from the first hiding session better than they do those of the second hiding session, suggesting their memories may be reinforced during the second hiding session. We also investigated how well episodic memory performance predicted performance on the three aspects of the WWW memory task separately. In the Passive treatment, episodic memory performance predicts performance on all three aspects of the WWW memory task equally. However, in the Active treatment it only predicts performance on the what component. This could imply that during active encoding a different memory system is used for where and when information than during passive encoding. Encoding of what information seems to rely on episodic memory processing in both conditions.

Spatial context is a defining feature of episodic memories, which are often characterized as being events occurring in specific spatiotemporal contexts. In this review, I summarize research suggesting a common neural basis for episodic and spatial memory and relate this to the role of spatial context in episodic memory. I review evidence that spatial context serves as a scaffold for episodic memory and imagination, in terms of both behavioral and neural effects demonstrating a dependence of episodic memory on spatial representations. These effects are mediated by a posterior-medial set of neocortical regions, including the parahippocampal cortex, retrosplenial cortex, posterior cingulate cortex, precuneus, and angular gyrus, which interact with the hippocampus to represent spatial context in remembered and imagined events. I highlight questions and areas that require further research, including differentiation of hippocampal function along its long axis and subfields, and how these areas interact with the posterior-medial network. This article is categorized under: Psychology > Memory Neuroscience > Cognition.

Human episodic memory is supported by networks of white matter tracts that connect frontal, temporal, and parietal regions. Degradation of white matter microstructure is increasingly recognized as a general mechanism of cognitive deterioration with aging. However, atrophy of gray matter regions also occurs and, to date, the potential role of specific white matter connections has been largely ignored. Changes to frontotemporal tracts may be important for the decline of episodic memory; while frontotemporal cooperation is known to be critical, the precise pathways of interaction are unknown. Diffusion-weighted MRI tractography was used to reconstruct three candidate fasciculi known to link components of memory networks: the fornix, the parahippocampal cingulum, and the uncinate fasciculus. Age-related changes in the microstructure of these tracts were investigated in 40 healthy older adults between the ages of 53 and 93 years. The relationships between aging, microstructure, and episodic memory were assessed for each individual tract. Age-related reductions of mean fractional anisotropy and/or increased mean diffusivity were found in all three tracts. However, age-related decline in recall was specifically associated with degradation of fornix microstructure, consistent with the view that this tract is important for episodic memory. In contrast, a decline in uncinate fasciculus microstructure was linked to impaired error monitoring in a visual object-location association task, echoing the effects of uncinate transection in monkeys. These results suggest that degradation of microstructure in the fornix and the uncinate fasciculus make critical but differential contributions to the mechanisms underlying age-related cognitive decline and subserve distinct components of memory.

Testing episodic memory in animals: A new approach

Tulving (1972) defined episodic memory as memory for what, where, and when. Clayton and Dickinson’s (1998) behavioral model for animals was adapted to examine what, where, and when memory in humans. Participants viewed unique visual scenes of furnished homes in both blocked and mixed designs. They were tested separately for memory of objects (What), spatial configurations (Where), and temporal order of the scenes (When), and participants’ accuracy and reaction times were examined for each condition. Performance was highest and reaction time was fastest for the What condition. Participants were also faster and more accurate in the mixed design experiment compared to the blocked design experiment. This study established a behavioral analysis of episodic memory in humans based upon Clayton and Dickinson’s (1998) animal model, which will provide a basis for functional episodic memory studies to separately characterize the cortical mechanisms for processing episodic memory using the object, spatial, and temporal task with humans.

We have investigated the cortical efferent projections of the macaque monkey retrosplenial and posterior cingulate cortices by using (3)H-amino acids as anterograde tracers. All the injections produced extensive local connections to other portions of this region. There were also a number of extrinsic efferent cortical connections, many of which have not hitherto been reported. Major projections from the retrosplenial cortex were directed to the frontal lobe, with heaviest terminations in areas 46, 9, 10, and 11. There were also very substantial projections to the entorhinal cortex, presubiculum, and parasubiculum of the hippocampal formation, as well as to areas TH and TF of the parahippocampal cortex. Some injections led to labeling of area V4, the dorsal bank of the superior temporal sulcus, and area 7a of the parietal cortex. Projections from the posterior cingulate cortex innervated all these same regions, although the density of termination was different from the retrosplenial projections. The posterior cingulate cortex gave rise to additional projections to parietal area DP and to the cortex along the convexity of the superior temporal gyrus. The ventral portion of the posterior cingulate cortex (area 23v) gave rise to much denser efferent projections to the hippocampal formation than the dorsal portions (areas 23e and i). These connections are discussed in relation to the clinical syndromes of retrosplenial amnesia and topographic disorientation in humans commonly caused by lesions in the caudoventral portions of the retrosplenial and posterior cingulate cortices.

A novel experimental approach to episodic memory in humans based on the privileged access of odors to memories

Human beings with damage to the mammillary bodies exhibit episodic memory disruption. This study investigated the potential participation of the medial mammillary nucleus (MM), a structure that receives a high density of melaninconcentrating hormone immunoreactive fibers (MCH) potentially involved in food intake, in processes of retrieval of memory about places where food was previously found, in rats. In addition, we investigated the possible involvement of this brain structure in both aversively motivated spatial memory, using the Morris water maze, and in anxiety, using the elevated plus maze. A behavioral task involving search for food guided by spatial memory, in rats, functionally analogous to the paired-associate learning task used for studying episodic memory in humans, was described. Rats trained to dig for food in an arena were exposed both to the pairing of a taste, peanut, with a specific place in the arena and, in a second trial, to the pairing of another taste, hazelnut, with another place in the arena. Immediately before a third trial, while still in the "waiting box", the animals received a "sample" of either peanut or hazelnut. Then, they were inserted into the arena for a third trial and could search and dig for food buried in the place previously associated with the sample. The taste-place associations, sequence of associations, pairing places and sample offered before the third trial, were all varied quasi-randomly every day. The animals took extensive training to learn this task. It was found that the number of visits and the time spent in the place indicated by the sample were significantly greater as compared to the corresponding parameters of the place previously associated with a taste but not indicated by the sample, when the time interval between the second and the third trials was both 60 and 120 min; probe tests with no food in the arena in the third trial allowed to exclude the hypothesis that the rats were performing the task relying on olfactory cues, leading to the conclusion that the animals performed the task relying on the memory for the associations tastefood. Rats with selective damage to the MM, induced by topic, microiontophoretic, injections of N-Methyl-D-Aspartate (NMDA), tested in the taste-place pairedassociate learning task, did not exhibit any disruption of performance relative to the controls. Additional analyses revealed that both MM and control subjects exhibited a reduction of food search during the post-operatory tests as compared to their own performance in pre-operatory tests; however, this reduction was stronger towards the place indicated by the sample, particularly for the animals subjected to MM damage.

Induction and measurement of episodic memories in healthy adults

Abstract. Individuals between the ages of 18 and 94 (N = 326) completed a battery of episodic memory tasks, as well as several measures of spatial visualization. A female advantage in verbal episodic memory and a male advantage in spatial and visual episodic memory were observed. Mediation analyses provided evidence that performance on spatial visualization tasks greatly influences the magnitude of the effect for sex differences among the different episodic memory constructs. In particular, the spatial visualization construct fully mediated the relationship between sex and episodic spatial memory performance. Further, when spatial visualization was included as a mediator in the model the relationship between sex and episodic verbal memory increased, and the relationship between sex and episodic visual memory reversed, such that women scored higher than men.

Mental time travel is defined as the human ability to remember unique personal past experiences (episodic memory) and to anticipate and plan future events. Considerable debate has arisen around the question of whether nonhuman animals are also capable of mental time travel, ranging from complete denial of the ability in nonhumans to the suggestion that they have episodic memory and readily plan for the future. We evaluate the current evidence available from comparative cognition experiments and human-developmental research. Studies of episodic-like memory in birds and nonhuman mammals have centered on their ability to remember what, where, and when a single event occurred. Although clear evidence for memory of what and where has been shown, memory of when does not always appear and may depend on both the species tested and the experimental design used. We argue for a clear distinction between remembering when in absolute time an event occurred and remembering how long ago it occurred. Studies of neural processes indicate that the hippocampus is necessary for episodic memory in humans and episodic-like memory in rats. It is argued that studies of nonhumans should not focus on presence versus absence of human traits but should examine alternative mental time travel abilities in animals that may have evolved independently as adaptations to a particular ecological niche.

Episodic memory: what can animals remember about their past?

The human hippocampus is a brain region that supports episodic and spatial memory. Recent experiments have drawn on animal research and computational modelling to reveal how the unique computations and representations of the hippocampus support episodic and spatial memory. Invasive electrophysiological recordings and non-invasive functional brain imaging have provided evidence for the rapid formation of hippocampal representations, as well as the ability of the hippocampus to both pattern-separate and pattern-complete input from the neocortex. Further, recent evidence has shown that hippocampal representations are in constant flux, undergoing a continual process of strengthening, weakening and altering. This research offers a glimpse into the highly plastic and flexible nature of the human hippocampal system in relation to episodic memory.