Hippocampal place-cell sequences depict future paths to remembered goals

Solomon H Snyder Department of Neuroscience, Johns Hopkins University School Of Medicine, Baltimore, Maryland 21205, USA.
Nature (Impact Factor: 41.46). 04/2013; 497(7447). DOI: 10.1038/nature12112
Source: PubMed


Effective navigation requires planning extended routes to remembered goal locations. Hippocampal place cells have been proposed to have a role in navigational planning, but direct evidence has been lacking. Here we show that before goal-directed navigation in an open arena, the rat hippocampus generates brief sequences encoding spatial trajectories strongly biased to progress from the subject's current location to a known goal location. These sequences predict immediate future behaviour, even in cases in which the specific combination of start and goal locations is novel. These results indicate that hippocampal sequence events characterized previously in linearly constrained environments as 'replay' are also capable of supporting a goal-directed, trajectory-finding mechanism, which identifies important places and relevant behavioural paths, at specific times when memory retrieval is required, and in a manner that could be used to control subsequent navigational behaviour.

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    • "When rats are tested in a multiple-choice-point T-maze, place cell ensemble activity " flows " down each arm, often ahead of the animal's current position ( Johnson & Redish 2007), suggesting that the animals may be imagining the outcome of each arm choice. This possibility is strengthened by recent findings that place cell firing sequences are predominant during the early stages of learning and predict immediate future behavior in an open field with multiple start and goal locations (Pfeiffer & Foster 2013, Singer et al. 2013). These findings provide evidence at the level of neuronal activity that fits with behavior seen in rodents at choice points, namely vicarious trial and error (VTE). "
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    • "It is commonly assumed that place cells provide a representation of the environment that is used for spatially guided behavior. Early work indicated that place cells predicted the animal's choice of a goal arm on a maze (O'Keefe and Speakman, 1987), and subsequent work has shown this to be the case in identifying reward locations (Lenk-Santini et al., 2002) and in the planning of routes (Pfeiffer and Foster, 2013). If the hippocampus provides a neural substrate for spatial and episodic memory (O'Keefe and Nadel, 1978; Poucet, 1993; Morris and Frey, 1997; Eichenbaum et al., 1999; Wood et al., 1999), then when there is place field repetition, animals should have difficulty discriminating between individual compartments . "
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    ABSTRACT: Recent studies have shown that place cells in the hippocampus possess firing fields that repeat in physically similar, parallel environments. These results imply that it should be difficult for animals to distinguish parallel environments at a behavioral level. To test this, we trained rats on a novel odor-location task in an environment with four parallel compartments which had previously been shown to yield place field repetition. A second group of animals was trained on the same task, but with the compartments arranged in different directions, an arrangement we hypothesised would yield less place field repetition. Learning of the odor-location task in the parallel compartments was significantly impaired relative to learning in the radially arranged compartments. Fewer animals acquired the full discrimination in the parallel compartments compared to those trained in the radial compartments, and the former also required many more sessions to reach criterion compared to the latter. To confirm that the arrangement of compartments yielded differences in place cell repetition, in a separate group of animals we recorded from CA1 place cells in both environments. We found that CA1 place cells exhibited repeated fields across four parallel local compartments, but did not do so when the same compartments were arranged radially. To confirm that the differences in place field repetition across the parallel and radial compartments depended on their angular arrangement, and not incidental differences in access to an extra-maze visual landmark, we repeated the recordings in a second set of rats in the absence of the orientation landmark. We found, once again, that place fields showed repetition in parallel compartments, and did not do so in radially arranged compartments. Thus place field repetition, or lack thereof, in these compartments was not dependent on extra-maze cues. Together, these results imply that place field repetition constrains spatial learning.
    Hippocampus 08/2015; 00:1-17. · 4.16 Impact Factor
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    • "Interestingly, recent data indicates that place cell ripple related preplay can include novel routes (O ´ lafsdó ttir et al., 2015)—a key property of vector navigation . However, the linear look-ahead model proposes activity sweeps along two non-collinear axes, not necessarily oriented toward the goal, in contrast to reports of goal-directed preplay (Pfeiffer and Foster, 2013). "
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    ABSTRACT: Mammals are able to navigate to hidden goal locations by direct routes that may traverse previously unvisited terrain. Empirical evidence suggests that this "vector navigation" relies on an internal representation of space provided by the hippocampal formation. The periodic spatial firing patterns of grid cells in the hippocampal formation offer a compact combinatorial code for location within large-scale space. Here, we consider the computational problem of how to determine the vector between start and goal locations encoded by the firing of grid cells when this vector may be much longer than the largest grid scale. First, we present an algorithmic solution to the problem, inspired by the Fourier shift theorem. Second, we describe several potential neural network implementations of this solution that combine efficiency of search and biological plausibility. Finally, we discuss the empirical predictions of these implementations and their relationship to the anatomy and electrophysiology of the hippocampal formation. Copyright © 2015 The Authors. Published by Elsevier Inc. All rights reserved.
    Neuron 08/2015; 87(3):507-20. DOI:10.1016/j.neuron.2015.07.006 · 15.05 Impact Factor
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