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: 42.35). 04/2013; 497(7447). DOI: 10.1038/nature12112
Source: PubMed

ABSTRACT 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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    • "Decision-making based on visual perception not only anticipates rewards but also takes into account risks and possible, future harms (Fleming, Whiteley et al. 2010). As discussed earlier, hippocampal simulations do not always replicate past experiences, they can depict never-experienced, novel combinations of past events (Gupta, van der Meer et al. 2010), reinforcing the notion that animals are capable of inference (Tolman 1948; Pfeiffer and Foster 2013), through using configural, as opposed to elemental, associations (Honey, Iordanova et al. 2014). "
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    ABSTRACT: This article argues both rapid eye movement (REM) and non-rapid eye movement (NREM) sleep contribute to overnight episodic memory processes but their roles differ. Episodic memory may have evolved from memory for spatial navigation in animals and humans. Equally, mnemonic navigation in world and mental space may rely on fundamentally equivalent processes. Consequently, the basic spatial network characteristics of pathways which meet at omnidirectional nodes or junctions may be conserved in episodic brain networks. A pathway is formally identified with the unidirectional, sequential phases of an episodic memory. In contrast, the function of omnidirectional junctions is not well understood. In evolutionary terms, both animals and early humans undertook tours to a series of landmark junctions, to take advantage of resources (food, water and shelter), whilst trying to avoid predators. Such tours required memory for emotionally significant landmark resource-place-danger associations and the spatial relationships amongst these landmarks. In consequence, these tours may have driven the evolution of both spatial and episodic memory. The environment is dynamic. Resource-place associations are liable to shift and new resource-rich landmarks may be discovered, these changes may require re-wiring in neural networks. To realise these changes, REM may perform an associative, emotional encoding function between memory networks, engendering an omnidirectional landmark junction which is instantiated in the cortex during NREM Stage 2. In sum, REM may preplay associated elements of past episodes (rather than replay individual episodes), to engender an unconscious representation which can be used by the animal on approach to a landmark junction in wake. Copyright © 2015. Published by Elsevier Inc.
    Neurobiology of Learning and Memory 04/2015; 122. DOI:10.1016/j.nlm.2015.04.005 · 4.04 Impact Factor
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    • "Such activation patterns may relate to the forward sweeps of activity observed during travel periods ( Johnson et al . , 2007 ; Wikenheiser and Redish , 2015 ) or brief ensemble spiking events ( Pfeiffer and Foster , 2013 ) . More explicitly , Wikenheiser and Redish ( 2015 ) have shown that the activity prior to running to a goal is related to the distance to that goal . "
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    ABSTRACT: Adapting behavior to accommodate changes in the environment is an important function of the nervous system. A universal problem for motile animals is the discovery that a learned route is blocked and a detour is required. Given the substantial neuroscience research on spatial navigation and decision-making it is surprising that so little is known about how the brain solves the detour problem. Here we review the limited number of relevant functional neuroimaging, single unit recording and lesion studies. We find that while the prefrontal cortex (PFC) consistently responds to detours, the hippocampus does not. Recent evidence suggests the hippocampus tracks information about the future path distance to the goal. Based on this evidence we postulate a conceptual model in which: Lateral PFC provides a prediction error signal about the change in the path, frontopolar and superior PFC support the re-formulation of the route plan as a novel subgoal and the hippocampus simulates the new path. More data will be required to validate this model and understand (1) how the system processes the different options; and (2) deals with situations where a new path becomes available (i.e., shortcuts).
    Frontiers in Human Neuroscience 04/2015; 9. DOI:10.3389/fnhum.2015.00125 · 2.90 Impact Factor
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    • "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. In many of the events, the sequence of active cells began at the current location and ended at the goal location , followed by the animal taking the path defined by the place-cell activity. "
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    ABSTRACT: 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. Copyright © 2015 Cold Spring Harbor Laboratory Press; all rights reserved.
    Cold Spring Harbor Perspectives in Medicine 02/2015; 5(1):a021808. DOI:10.1101/cshperspect.a021808 · 7.56 Impact Factor
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