Awake replay of remote experiences in the hippocampus

Karlsson, Matts; Frank, Loren M.

doi:10.1038/nn.2344

Cited by 695 publications

(913 citation statements)

References 37 publications

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“…This view may be supported by studies which have indicated that patterned replay can occur for hours (e.g. Karlsson & Frank, 2009) and up to a day (Kudirmoti et al, 1999) after training. If a short period of recurrent activation is necessary to consolidate an extra-hippocampal trace for some tasks, this is consistent with the observation that span of temporally graded amnesia in flavor/odor cued conditioning is 1-2 days (Clark et al, 2002;Tse et al, 2007;Winocur et al, 2001;Winocur, 1990).…”

Section: Histologymentioning

confidence: 88%

Time course of dorsal and ventral hippocampal involvement in the expression of trace fear conditioning

Cox

Czerniawski

Ree

et al. 2013

Neurobiology of Learning and Memory

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It is becoming increasingly clear that the time-dependent involvement of the hippocampus in the recall of acquired behaviors is more complicated than once thought.Several early studies demonstrated that hippocampal damage attenuates the expression of recent, but not remotely trained tasks. By contrast, an emerging body of evidence has shown that damage to, or inactivation of, the hippocampus impairs recall across a wide range of training-testing intervals. Collectively, these data suggest that the time course of hippocampal involvement in the storage or recall of previouslyacquired memories differs according to hippocampal subregion and the particular learning task under consideration. The present study examined the contributions of dorsal (DH) and ventral (VH) hippocampus to the expression of previously-acquired trace fear conditioning, a form of Pavlovian conditioning in which the presentation of an initially neutral cue or cues and a subsequent aversive stimulus is separated by a nostimulus (trace) interval. Specifically, either the GABA-A agonist muscimol or saline was ii infused into the DH or VH prior to testing 1, 7, 28, or 42 days after trace fear conditioning. The results revealed a marked dissociation: pre-testing inactivation of DH failed to impair performance at any time-point, while pre-testing inactivation of VH impaired performance at all time-points. Importantly, pre-testing inactivation of VH had no effect on the performance during testing of previously-acquired delay conditioning.Collectively, these data suggest that VH, but not DH, remains a neuroanatomical locus critical to the recall or expression of trace fear conditioning over an extended period of time.

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Section: Histologymentioning

confidence: 88%

Time course of dorsal and ventral hippocampal involvement in the expression of trace fear conditioning

Cox

Czerniawski

Ree

et al. 2013

Neurobiology of Learning and Memory

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“…Studies in human subjects show that overlapping hippocampal networks are activated during episodic recall and imagination of fictitious experiences (Hassabis et al 2007). In animals, sharp-wave ripples can activate cells along both past and future trajectories (Karlsson and Frank 2009;Gupta et al 2010;Pfeiffer and Foster 2013). Pfeiffer and Foster (2013), for example, trained rats to find a rewarded well within a large environment while sharp-wave ripple-associated replay events were recorded in the hippocampus.…”

Section: Memory Consolidation and Retrievalmentioning

confidence: 99%

Place Cells, Grid Cells, and Memory

Moser

Rowland

Moser

2015

Cold Spring Harb Perspect Biol

425

267

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The hippocampal system is critical for storage and retrieval of declarative memories, including memories for locations and events that take place at those locations. Spatial memories place high demands on capacity. Memories must be distinct to be recalled without interference and encoding must be fast. Recent studies have indicated that hippocampal networks allow for fast storage of large quantities of uncorrelated spatial information. The aim of the this article is to review and discuss some of this work, taking as a starting point the discovery of multiple functionally specialized cell types of the hippocampal-entorhinal circuit, such as place, grid, and border cells. We will show that grid cells provide the hippocampus with a metric, as well as a putative mechanism for decorrelation of representations, that the formation of environment-specific place maps depends on mechanisms for long-term plasticity in the hippocampus, and that long-term spatiotemporal memory storage may depend on offline consolidation processes related to sharp-wave ripple activity in the hippocampus. The multitude of representations generated through interactions between a variety of functionally specialized cell types in the entorhinal-hippocampal circuit may be at the heart of the mechanism for declarative memory formation.T he scientific study of human memory started with Herman Ebbinghaus, who initiated the quantitative investigation of associative memory processes as they take place (Ebbinghaus 1885). Ebbinghaus described the conditions that influence memory formation and he determined several basic principles of encoding and recall, such as the law of frequency and the effect of time on forgetting. With Ebbinghaus, higher mental functions were brought to the laboratory. In parallel with the human learning tradition that Ebbinghaus started, a new generation of experimental psychologists described the laws of associative learning in animals. With behaviorists like Pavlov, Watson, Hull, Skinner, and Tolman, a rigorous program for identifying the laws of animal learning was initiated. By the middle of the 20th century, a language for associative learning processes had been developed, and many of the fundamental relationships between environment and behavior had been described. What was completely missing, though, was an understanding of the neural activity underlying the formation of the memory. The behaviorists had deliberately shied away from physiological explanations because of the intangible nature of neural activity at that time.Then the climate began to change. Karl Lashley had shown that lesions in the cerebral cortex had predictable effects on behavior in Editors: Eric R. Kandel, Yadin Dudai, and Mark R. Mayford Additional Perspectives on Learning and Memory available at

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“…When we discuss the duration of a memory trace, we mean that this trace is maintained (e.g. by spontaneous replay during sleep (Wilson & Mcnaughton 1994) or waking (Karlsson & Frank 2009) or other mechanisms) without retrieving the cache and either leaving the item in place or rehoarding it (Grubb & Pravosudov 1994). Maintenance could happen by travelling through the area where caches are located, and then triggering the memories for the cache locations, which are thereby reconsolidated (Nader et al 2000a,b).…”

Section: Using Ecology To Predict Specific Memory Adaptationsmentioning

confidence: 99%

Using ecology to guide the study of cognitive and neural mechanisms of different aspects of spatial memory in food-hoarding animals

Smulders

Gould

Leaver

2010

Phil. Trans. R. Soc. B

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Understanding the survival value of behaviour does not tell us how the mechanisms that control this behaviour work. Nevertheless, understanding survival value can guide the study of these mechanisms. In this paper, we apply this principle to understanding the cognitive mechanisms that support cache retrieval in scatter-hoarding animals. We believe it is too simplistic to predict that all scatter-hoarding animals will outperform non-hoarding animals on all tests of spatial memory. Instead, we argue that we should look at the detailed ecology and natural history of each species. This understanding of natural history then allows us to make predictions about which aspects of spatial memory should be better in which species. We use the natural hoarding behaviour of the three best-studied groups of scatter-hoarding animals to make predictions about three aspects of their spatial memory: duration, capacity and spatial resolution, and we test these predictions against the existing literature. Having laid out how ecology and natural history can be used to predict detailed cognitive abilities, we then suggest using this approach to guide the study of the neural basis of these abilities. We believe that this complementary approach will reveal aspects of memory processing that would otherwise be difficult to discover.

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Awake replay of remote experiences in the hippocampus

Cited by 695 publications

References 37 publications

Time course of dorsal and ventral hippocampal involvement in the expression of trace fear conditioning

Time course of dorsal and ventral hippocampal involvement in the expression of trace fear conditioning

Place Cells, Grid Cells, and Memory

Using ecology to guide the study of cognitive and neural mechanisms of different aspects of spatial memory in food-hoarding animals

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