Experience-dependent, asymmetric expansion of hippocampal place fields

Mehta, Mayank R.; Barnes, Carol A.; McNaughton, Bruce L.

doi:10.1073/pnas.94.16.8918

Cited by 449 publications

(503 citation statements)

References 17 publications

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“…Non-spatial hippocampal correlates can be explained. Place cell recordings are examining detailed quantitative second-order properties of the tuning curves, including both spatial [39,112,151,174,208] (to list only a few) and non-spatial [11,94,247], and these properties are being modeled at a quantitative level [16,172,196,205]. Detailed explanations of hippocampal roles in both spatial and non-spatial tasks are available [72,173,196,225].…”

Section: Resultsmentioning

confidence: 99%

The hippocampal debate: are we asking the right questions?

Redish

2001

Behavioural Brain Research

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For years, the debate has been: 'Is the hippocampus the cognitive map?' or 'Is the hippocampus the core of memory?' These two hypotheses derived their original power from two key experiments-the cognitive map theory from the remarkable spatial correlates seen in recordings of hippocampal pyramidal cells and the memory theory from the profound amnesias seen in the patient H.M. Both of these key experiments have been reinterpreted over the years: hippocampal cells are correlated with much more than place and H.M. is missing much more than just his hippocampus. However, both theories are still debated today. The hippocampus clearly plays a role in both navigation and memory processing. The question that must be addressed is rather: 'What is the role played by the hippocampus in the navigation and memory systems?' By looking at the navigation system as a whole, one can identify the major role played by the hippocampus as correcting for accumulation errors that occur within idiothetic navigation systems. This is most clearly experimentally evident as reorientation when an animal is lost. Carrying this over to a more general process, this becomes a role of recalling a context, bridging a contextual gap, or, in other words, it becomes a form of recognition memory. I will review recent experimental data which seems to support this theory over the more general spatial or memory theories traditionally applied to hippocampus.

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Section: Resultsmentioning

confidence: 99%

The hippocampal debate: are we asking the right questions?

Redish

2001

Behavioural Brain Research

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“…We conjecture that repeated pairing of different streams of input could generate robust associations between them through rapid Hebbian synaptic plasticity, resulting in stable spatial representations 48 and increased firing rates 19,[48][49][50] . Under this model, during random foraging in RW, distal visual cues are paired repeatedly with the same constellation of proximal cues at each location, resulting in a place code.…”

Section: Discussionmentioning

confidence: 99%

“…In the systematicpillar task, when we paired locomotion and visual cues repeatedly, this selectivity was strengthened and extended to the middle of the paths. Restricting the analysis to cells that fired on at least two nonoverlapping arms on the three-pillar task revealed that these cells exhibited a disto-code 21 , which is a specific case of the more general distance selectivity observed in the goal-directed tasks.We conjecture that repeated pairing of different streams of input could generate robust associations between them through rapid Hebbian synaptic plasticity, resulting in stable spatial representations 48 and increased firing rates 19,[48][49][50] . Under this model, during random foraging in RW, distal visual cues are paired repeatedly with the same constellation of proximal cues at each location, resulting in a place code.…”

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confidence: 98%

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

et al. 2014

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During real-world (RW) exploration, rodent hippocampal activity shows robust spatial selectivity, which is hypothesized to be governed largely by distal visual cues, although other sensory-motor cues also contribute. Indeed, hippocampal spatial selectivity is weak in primate and human studies that use only visual cues. To determine the contribution of distal visual cues only, we measured hippocampal activity from body-fixed rodents exploring a two-dimensional virtual reality (VR). Compared to that in RW, spatial selectivity was markedly reduced during random foraging and goal-directed tasks in VR. Instead we found small but significant selectivity to distance traveled. Despite impaired spatial selectivity in VR, most spikes occurred within ~2-s-long hippocampal motifs in both RW and VR that had similar structure, including phase precession within motif fields. Selectivity to space and distance traveled were greatly enhanced in VR tasks with stereotypical trajectories. Thus, distal visual cues alone are insufficient to generate a robust hippocampal rate code for space but are sufficient for a temporal code. npg © 2015 Nature America, Inc. All rights reserved.1 2 2 VOLUME 18 | NUMBER 1 | JANUARY 2015 nature neurOSCIenCe a r t I C l e S same physical location in space can be approached from multiple different directions at different speeds. We thus investigated the contribution of distal visual cues only in determining selectivity in such an experimental setup. RESULTS Nature of spatial selectivity of hippocampal responsesWe measured hippocampal activity during a two-dimensional randomforaging task in RW and VR [35][36][37] with similar distal visual cues (Fig. 1a). In VR, the rats were body-fixed, i.e., their bodies were held in place, with a harness on a floating ball, allowing for head movements but precluding full-body turns, thus minimizing vestibular cues (Online Methods) 21,36 . Rats quickly learned to avoid the virtual edges entirely on the basis of visual cues 36 and spent a similar amount of time away from the edges and in the center of the platform (Fig. 1a) compared to in RW. We measured the activity of 1,066 and 1,238 principal neurons in RW and VR, respectively, in the dorsal CA1 of four rats under a variety of conditions (Online Methods). Neurons fired vigorously in restricted regions of space in RW, as expected (Fig. 1b,c, Supplementary Fig. 1a and Supplementary Video 1) 1 . In contrast, the neurons showed little spatial selectivity in VR during random foraging (Fig. 1b,d and Supplementary Fig. 1b).Across the ensemble, neurons had moderately reduced (25%) mean firing rates but greatly reduced (68%) peak firing rates in VR ( Fig. 2a and Supplementary Fig. 2a). Neurons in VR also had greatly reduced spatial information content (75%), stability (59%), sparsity (42%) and coherence (40%) (Fig. 2b-d and Supplementary Fig. 2b,c) compared to spatially localized, stable and sparse RW rate maps (Fig. 2c). Although the mean firing rate was inversely correlated with information content (Supplementary Fig. 2d)...

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“…Our choice of such a model reflects our belief that the place-cell population represents a large scale, unitary construct, the environment, rather than an agglomeration of separate, smaller-scale features of the environment such as pairwise relationships between objects (O'Keefe and Conway 1978; Hetherington and Shapiro 1997; but see Shapiro et al 1997; Wood et al 1999). In part, this view is based on the notion that place cells (especially CA3 place cells) interact with each other and are not a set of independent feature detectors (Muller et al 1991, Muller et al 1996; Blum and Abbott 1996; Mehta et al 1997; Samsonovich and McNaughton 1997). It is our contention that connections among place cells will prove to be the essential feature that allows the place-cell ensemble to be used in navigation.…”

Section: Discussionmentioning

confidence: 99%

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

Fenton

Csizmadia

Muller

2000

The Journal of General Physiology

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Changing the angular separation between two visual stimuli attached to the wall of a recording cylinder causes the firing fields of place cells to move relative to each other, as though the representation of the floor undergoes a topological distortion. The displacement of the firing field center of each cell is a vector whose length is equal to the linear displacement and whose angle indicates the direction that the field center moves in the environment. Based on the observation that neighboring fields move in similar ways, whereas widely separated fields tend to move relative to each other, we develop an empirical vector-field model that accounts for the stated effects of changing the card separation. We then go on to show that the same vector-field equation predicts additional aspects of the experimental results. In one example, we demonstrate that place cell firing fields undergo distortions of shape after the card separation is changed, as though different parts of the same field are affected by the stimulus constellation in the same fashion as fields at different locations. We conclude that the vector-field formalism reflects the organization of the place-cell representation of the environment for the current case, and through suitable modification may be very useful for describing motions of firing patterns induced by a wide variety of stimulus manipulations.

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Experience-dependent, asymmetric expansion of hippocampal place fields

Cited by 449 publications

References 17 publications

The hippocampal debate: are we asking the right questions?

The hippocampal debate: are we asking the right questions?

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

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