Long-term plasticity in hippocampal place-cell representation of environmental geometry

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

doi:10.1038/416090a

Cited by 427 publications

(465 citation statements)

References 27 publications

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“…Path-dependence (Frank et al, 2000;Wood et al, 2000), including retrospective coding, is another such example of a situation where position is not sufficient to predict the firing of "place cells." Similarly, the finding that the responses of place cells depend on the behavioral context (Markus, Qin, Leonard, et al, 1995) and the finding that similar responses take place in different environments (Lever et al, 2002) argue against a perfectly accurate hippocampal place code.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

Howard¹,

Fotedar²,

Datey³

et al. 2005

Psychological Review

273

334

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The medial temporal lobe (MTL) has been studied extensively at all levels of analysis, yet its function remains unclear. Theory regarding the cognitive function of the MTL has centered along 3 themes. Different authors have emphasized the role of the MTL in episodic recall, spatial navigation, or relational memory. Starting with the temporal context model (M. W. Howard and M. J. , a distributed memory model that has been applied to benchmark data from episodic recall tasks, the authors propose that the entorhinal cortex supports a gradually changing representation of temporal context and the hippocampus proper enables retrieval of these contextual states. Simulation studies show this hypothesis explains the firing of place cells in the entorhinal cortex and the behavioral effects of hippocampal lesion in relational memory tasks. These results constitute a first step towards a unified computational theory of MTL function that integrates neurophysiological, neuropsychological and cognitive findings.The medial temporal lobe (MTL) is a region that includes the hippocampus proper, the subicular complex and parahippocampal cortical regions, including entorhinal, perirhinal, and parahippocampal/postrhinal cortices. A great deal of data from neuropsychology (e.g. Eichenbaum & Cohen, 2001;Scoville & Milner, 1957;Squire, 1992) and functional imaging (e.g. Fernandez, Effern, Grunwald, et al., 1999;Stern, Corkin, Gonzalez, et al., 1996;Wagner et al., 1998) has converged on the idea that the MTL is important in learning and memory. In order to bridge the gap between cognition and cellular-level physiology, we need a mechanistic, mesoscopic description of MTL computational function. We already have several successful verbally-formulated theories of the cognitive function of the MTL. These are described in turn in the following subsections. This paper will attempt to draw these multiple verbal theories together into a single computational framework that is consistent with known neurophysiological and neuroanatomical data.

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Section: Discussionmentioning

confidence: 99%

“…Open Field Methods-The cellular simulation was presented separately with a series of positions and head directions collected by Lever et al (2002) in a cylindrical environment and in a square environment. 15 Position and head direction were sampled at 50 Hz for ten minutes.…”

Section: Applications: the Open Fieldmentioning

confidence: 99%

The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

Howard¹,

Fotedar²,

Datey³

et al. 2005

Psychological Review

273

334

View full text Add to dashboard Cite

show abstract

“…When an animal in the open field starts a sequence of stereotyped movements, the firing of hippocampal place fields changes (Markus, Qin, Leonard, et al, 1995). Further, if the movement of a rat is constrained to quadrants of an environment by means of barriers, the firing of hippocampal place cells is similar across the different quadrants (Lever, Wills, Cacucci, Burgess, & O'Keefe, 2002). Finally we note that the population vector method used here relies on an accurate measurement of low firing rates.…”

Section: Discussionmentioning

confidence: 99%

Place from time: Reconstructing position from a distributed representation of temporal context

Howard

Natu

2005

Neural Networks

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The temporal context model (TCM Howard & Kahana, 2002) was proposed to describe recency and associative effects observed in episodic recall. Episodic recall depends on an intact medial temporal lobe, a region of the brain that also supports a place code. Howard, Fotedar, Datey, and Hasselmo (2005) demonstrated that the leaky integrator that supports a gradually-changing representation of temporal context in TCM is sufficient to describe properties of cells observed in ventromedial entorhinal cortex during spatial navigation if it is provided with input about the animal's current velocity. This representation of temporal context generates noisy place cells in the open field, unlike the clearly-defined place cells observed in the hippocampus. Here we demonstrate that a reasonably accurate spatial representation can be extracted from temporal context with as few as eight cells, suggesting that the spatial precision observed in the place code in the hippocampus is not inconsistent with input from a representation of temporal-spatial context in entorhinal cortex.It has long been believed that the medial temporal lobe (MTL), including the hippocampus and parahippocampal cortical regions, is involved in episodic recall-memory for specific instances from ones' life (e. Keefe & Nadel, 1978;Eichenbaum, Dudchenko, Wood, Shapiro, & Tanila, 1999). Recently Howard et al. (2005) proposed that the temporal context model (TCM, Howard & Kahana, 2002) could provide a framework in which to describe aspects of both episodic recall and the construction and maintenance of a place code. We will review this work briefly here before presenting new results on the reconstruction of spatial position from a representation of temporal context. TCM (Howard & Kahana, 2002;Howard, 2004; Howard, Wingfield, & Kahana, Revised;Howard et al., 2005) provides a set of equations that describe a distributed representation of temporal context as a vector in a high-dimensional space. This model was developed to describe performance in situations in which a list of words are presented for a memory test. In TCM, the state of context at time step i, t i is updated according to where β is a free parameter that controls the rate of change of temporal context. The value of the scalar ρ i is chosen at each time step to keep the context vector of unit length. The context NIH Public Access TCM in episodic recall

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“…The notion of a cohesive attractor-based representation has also had to be modified in light of accumulating data suggesting that place cells do not always act as a unified population, but sometimes as a collection of independent individuals (O'Keefe and Burgess, 1996;Tanila et al, 1997;Skaggs and McNaughton, 1998;Jeffery, 2000;Lever et al, 2002). Furthermore, experiments with conflicting proximal and distal visual references showed not only that different subsets of place cells can be controlled by a different type of cues, but also that a small proportion of place fields split in half, each of the two halves responding to a different cue category (Knierim, 2002).…”

Section: Pi and The Representation Of Spacementioning

confidence: 99%

Path integration in mammals

2004

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ABSTRACT:It is often assumed that navigation implies the use, by animals, of landmarks indicating the location of the goal. However, many animals (including humans) are able to return to the starting point of a journey, or to other goal sites, by relying on self-motion cues only. This process is known as path integration, and it allows an agent to calculate a route without making use of landmarks. We review the current literature on path integration and its interaction with external, location-based cues. Special importance is given to the correlation between observable behavior and the activity pattern of particular neural cell populations that implement the internal representation of space. In mammals, the latter may well be the first high-level cognitive representation to be understood at the neural level.

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Long-term plasticity in hippocampal place-cell representation of environmental geometry

Cited by 427 publications

References 27 publications

The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

Place from time: Reconstructing position from a distributed representation of temporal context

Path integration in mammals

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