Development of the Hippocampal Cognitive Map in Preweanling Rats

Wills, Thomas J.; Cacucci, Francesca; Burgess, Neil; O’Keefe, John

doi:10.1126/science.1188224

Cited by 559 publications

(606 citation statements)

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“…Therefore, one of the neuronal characteristics most crucial and advanced in terms of echolocation processing seems to appear first and not last in the maturation hierarchy of AC. Our results from neonatal bats of two species adapted to different feeding and echolocation strategies emphasize that certain forms of neuronal circuitry for spatial orientation are implemented before their first use as it has also been suggested for hippocampal place units in rodents 21,22 . In bats, hippocampal place cells resemble those in rats quite well 23,24 and cortical delay-tuned neurons may constitute one of several input features for spatial representation and memory in hippocampus.…”

Section: Discussionsupporting

confidence: 52%

Auditory cortex of newborn bats is prewired for echolocation

et al. 2012

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neuronal computation of object distance from echo delay is an essential task that echolocating bats must master for spatial orientation and the capture of prey. In the dorsal auditory cortex of bats, neurons specifically respond to combinations of short frequency-modulated components of emitted call and delayed echo. These delay-tuned neurons are thought to serve in target range calculation. It is unknown whether neuronal correlates of active space perception are established by experience-dependent plasticity or by innate mechanisms. Here we demonstrate that in the first postnatal week, before onset of echolocation and flight, dorsal auditory cortex already contains functional circuits that calculate distance from the temporal separation of a simulated pulse and echo. This innate cortical implementation of a purely computational processing mechanism for sonar ranging should enhance survival of juvenile bats when they first engage in active echolocation behaviour and flight.

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Section: Discussionsupporting

confidence: 52%

Auditory cortex of newborn bats is prewired for echolocation

et al. 2012

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“…If place cells were generated exclusively from grid cells, grid and place cells would be expected to appear simultaneously in developing animals or with a faster time course for grid cells than place cells. Recordings from rat pups suggest that this is not the case (Langston et al 2010;Wills et al 2010). When pups leave the nest for the first time at 2-2.5 weeks of age, sharp and confined firing fields are present in a large proportion of the hippocampal pyramidal-cell population.…”

Section: Upstream Of Place Cells: Grid Cells and Other Cell Typesmentioning

confidence: 99%

Place Cells, Grid Cells, and Memory

Moser

Rowland

Moser

2015

Cold Spring Harb Perspect Biol

423

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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“…First, place cells in weanling rats show some adult-like spatial tuning during the animals' first spatial experience away from their nests, suggesting that spatial firing is an innate property of the network (10). Second, ensembles of place cells representing unvisited paths (11) or spaces (12) can become active during periods of rest or sleep before direct experience, a phenomenon called "preplay."…”

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confidence: 99%

A stable hippocampal representation of a space requires its direct experience

Rowland¹,

Yanovich

Kentros

2011

Proc. Natl. Acad. Sci. U.S.A.

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In humans and other mammals, the hippocampus is critical for episodic memory, the autobiographical record of events, including where and when they happen. When one records from hippocampal pyramidal neurons in awake, behaving rodents, their most obvious firing correlate is the animal's position within a particular environment, earning them the name "place cells." When an animal explores a novel environment, its pyramidal neurons form their spatial receptive fields over a matter of minutes and are generally stable thereafter. This experience-dependent stabilization of place fields is therefore an attractive candidate neural correlate of the formation of hippocampal memory. However, precisely how the animal's experience of a context translates into stable place fields remains largely unclear. For instance, we still do not know whether observation of a space is sufficient to generate a stable hippocampal representation of that space because the animal must physically visit a spot to demonstrate which cells fire there. We circumvented this problem by comparing the relative stability of place fields of directly experienced space from merely observed space following blockade of NMDA receptors, which preferentially destabilizes newly generated place fields. This allowed us to determine whether place cells stably represent parts of the environment the animal sees, but does not actually occupy. We found that the formation of stable place fields clearly requires direct experience with a space. This suggests that place cells are part of an autobiographical record of events and their spatial context, consistent with providing the "where" information in episodic memory.learning | plasticity | cognitive map | remapping | consolidation T he hippocampus is clearly central to mammalian learning and memory (1), and it is just as clear that an animal's position in space is by far the most obvious firing correlate of hippocampal neurons in awake, behaving rodents (2). However, the precise relationship between memory and place cells is less clear, making the study of the processes governing the formation of place fields particularly interesting. Consistent with the central role for the hippocampus in memory, the balance of experimental evidence supports the idea that place fields are constructed and stabilized by the animal's experience of that space. For example, place cells "remap" (i.e., change to unpredictable locations and/or change their firing rate) in response to even small changes in the sensory environment (3) or even changes in the animal's ongoing behavior (4, 5). Moreover, place fields are quite labile in novel environments until the animal has experienced the environment for several minutes (6, 7). Finally, inhibitors of synaptic plasticity prevent the long-term maintenance (i.e., destabilize) of place fields in novel but not familiar environments (8, 9).However, recent studies have forced a reexamination of the debate. First, place cells in weanling rats show some adult-like spatial tuning during the animals' first sp...

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Development of the Hippocampal Cognitive Map in Preweanling Rats

Cited by 559 publications

References 26 publications

Auditory cortex of newborn bats is prewired for echolocation

Auditory cortex of newborn bats is prewired for echolocation

Place Cells, Grid Cells, and Memory

A stable hippocampal representation of a space requires its direct experience

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