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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    • "We believe our work complements this approach. Short-wave ripple activity have been suggested to guide navigation (Johnson and Redish, 2007; Pfeiffer and Foster, 2013), but it occurs during sleep or when the rat is still (Foster and Wilson, 2006). Thus, while Erdem and Hasselmo (2014) work focuses on high level planning during key decision points, our model focuses on the decision making that takes place while the rat is in motion. "
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    ABSTRACT: There has been extensive research in recent years on the multi-scale nature of hippocampal place cells and entorhinal grid cells encoding which led to many speculations on their role in spatial cognition. In this paper we focus on the multi-scale nature of place cells and how they contribute to faster learning during goal-oriented navigation when compared to a spatial cognition system composed of single scale place cells. The task consists of a circular arena with a fixed goal location, in which a robot is trained to find the shortest path to the goal after a number of learning trials. Synaptic connections are modified using a reinforcement learning paradigm adapted to the place cells multi-scale architecture. The model is evaluated in both simulation and physical robots. We find that larger scale and combined multi-scale representations favor goal-oriented navigation task learning.
    Neural networks: the official journal of the International Neural Network Society 11/2015; DOI:10.1016/j.neunet.2015.09.006 · 2.71 Impact Factor
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    • "damagetothemedialentorhinalcortexshouldimpairthe processingofself-motioninformation,andthereforeshould resultinafurtherincreaseofthenumberofcontactswith theobjectlandmarkssoastorecalibrateself-localizationeven morefrequently.Third,thenumberofreplayepisodesand SWRsassociatedwithexploratorycontactswiththeobjects shouldbegreaterinthedarkthaninthelight.Againthis wouldoccurbecauseresettingcanbedoneeverywherewhen basedonvisuallandmarks,whileitcanoccuronlyatobject locationsinthedark.Ifreplayisthehallmarkoftheresetting process,thenitshouldincreaseatobjectlocationswhenthe ratistestedinthedark.Fourth,ifthetasequencesareof particularimportanceinshapingplacefieldactivitybasedon self-motioncues,inactivationofthemedialseptum,which disruptthetageneration,shouldresultinprofounddisruption ofhippocampalplacecellactivityindarknessbutnotin thelight(Wangetal.,2015).Lastly,animalswithdamaged medialentorhinalcortexshouldexpresslessreliablereplayasa consequenceofimpairedself-motionprocessing,particularlyin thedark. Recentprogressinunderstandingthephysiologicaland mechanisticaspectsofthenavigationalsysteminthebrainis tremendous.However,itisourcontentionthatthedetailed understandingofthebehavioralmechanismsunderpinnedby thesebrainprocesseshasnotbeenthesubjectofsomuch attention.Overall,wethinkthatthereisadeepneedfor re-assessingthefinestructureofthespatialbehaviorof theanimalinregisterwiththedischargepropertiesofcells carryingspatialsignals.Agoodillustrationofthetypeof analysisthatwouldbeusefulisprovidedbystudiesinwhich neuronalactivityisanalyzedinrelationtospecificbehaviors atspecificplaces,suchasdecisionpoints(e.g.,Johnsonand Redish,2007;Cataneseetal.,2012),specificlandmarkobjects (e.g.,Saveetal.,1998),goallocations(e.g.,Hoketal., 2007),aswellasduringperformanceofwell-designedspatial navigationtasks(e.g.,PfeifferandFoster,2013).Insuch away,itbecomespossibletodrawfunctionalrelationships betweencellfiringandcognitiveprocesseshypothesized tosupportself-localizationandnavigation.Althoughsuch correlationalapproachneedstobecomplementedbyanalyses ofcausalrelationships,webelievethatitisonlythrough adetaileddescriptionofactualspatialbehaviorthatwe canunderstandhowspatialnavigation,whichlooksso simpleatfirstsightbutissocomplexinreality,canbe implementedbythecoordinatedactivityofawidespreadbrain system. "
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    ABSTRACT: Since the discovery of place cells, the hippocampus is thought to be the neural substrate of a cognitive map. The later discovery of head direction cells, grid cells and border cells, as well as of cells with more complex spatial signals, has led to the idea that there is a brain system devoted to providing the animal with the information required to achieve efficient navigation. Current questioning is focused on how these signals are integrated in the brain. In this review, we focus on the issue of how self-localization is performed in the hippocampal place cell map. To do so, we first shortly review the sensory information used by place cells and then explain how this sensory information can lead to two coding modes, respectively based on external landmarks (allothetic information) and self-motion cues (idiothetic information). We hypothesize that these two modes can be used concomitantly with the rat shifting from one mode to the other during its spatial displacements. We then speculate that sequential reactivation of place cells could participate in the resetting of self-localization under specific circumstances and in learning a new environment. Finally, we provide some predictions aimed at testing specific aspects of the proposed ideas.
    Frontiers in Behavioral Neuroscience 10/2015; 9:292. DOI:10.3389/fnbeh.2015.00292 · 3.27 Impact Factor
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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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