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Hippocampal place-cell sequences depict future paths to remembered goals

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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Figure 1: Behaviour in the open-field spatial memory task.
Figure 2: Trajectory events.
Figure 3: Remote representation of goal location.
Figure 4: Representation of relevant vs. irrelevant locations.
Figure 5: Correspondence to past or future path.
Figure 6: Goal switching and flexibility in trajectory events.

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Acknowledgements

This work was supported by the Alfred P. Sloan Foundation, The Brain and Behavior Research Foundation (NARSAD Young Investigator Grant) and the National Institutes of Health grant MH085823.

Author information

Authors and Affiliations

Authors

Contributions

B.E.P. and D.J.F. designed the experiment and analyses, B.E.P. collected the data, B.E.P. and D.J.F. wrote the paper.

Corresponding author

Correspondence to David J. Foster.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-12 and Supplementary Table 1. (PDF 2041 kb)

Behavioural decoding accuracy during a representative epoch for rat 1, day 1

The video demonstrates the accuracy of position decoding during behaviour. Each frame depicts the predicted position of the rat (posterior probability) within the 2 m x 2 m arena given the unit firing patterns that occurred during that frame. The posterior probabilities are shown as a colourmap, which ranges from black (0) to white (0.1). Each frame represents 400 ms, and each frame is advanced from the previous by 100 ms. The rat's physical location and head direction are depicted by the cartoon white rat, and the locations of the 36 wells in the floor of the arena are shown as white squares. The HOME well location is coloured in cyan. If a RANDOM well is active (filled with chocolate) or if the rat is currently at the RANDOM well consuming the reward, it is coloured in green. If the HOME well is active or if the rat is currently at the HOME well consuming the reward, the previous RANDOM well is coloured in red. The time (from the beginning of the session) is depicted at the bottom of the video. (MOV 580 kb)

Representative trajectory events depicted in figure 2c demonstrating how the events progress across the arena through time

This video depicts three general 'types' of trajectory events: home-events (events which occur while the rat is at the HOME well), away-events (events which occur while the rat is away from the HOME well) that demonstrate a trajectory that ends at HOME, and away-events that demonstrate a trajectory that does not end at or cross HOME. Note the wide variety of paths encoded by the trajectory events and the smoothness of the trajectory. Each frame depicts the predicted position of the rat (posterior probability) within the 2 m x 2 m arena given the unit firing patterns that occurred during that frame. The posterior probabilities are shown as a colourmap, which ranges from black (0) to white (0.1). Each frame spans 20 ms, and is advanced from the previous by 5 ms. The time from the start of each event is depicted at the bottom of the video. The rat's physical position and head direction throughout each event are depicted by the cartoon white rat, and the locations of the 36 wells in the floor of the arena are shown as white squares. The HOME well location is coloured in cyan. If a RANDOM well is active (filled with chocolate) or if the rat is currently at the RANDOM well consuming the reward, it is coloured in green. If the HOME well is active or if the rat is currently at the HOME well consuming the reward, the previously active RANDOM well is coloured in red. The cyan line connects the peak posterior probabilities for each frame. At the end of each trajectory sequence, the entire event is shown collapsed across time as in Figure 2c. (MOV 7999 kb)

Representative episodes consisting of both exploratory behaviour and trajectory events

As video 1, but showing a representative episode consisting of both running periods and periods when the rat is stationary and trajectory events are occurring. Successive running and trajectory events within the episode are shown, allowing comparison between paths depicted by trajectory events and those previously and subsequently taken by the animal. During trajectory events, the speed of the video is slowed by a factor of 20 (each frame represents 20 ms, advanced in 5 ms increments) and a solid white border is drawn around the arena to indicate that the decoding is for a trajectory event rather than behaviour. Note that this video demonstrates trajectory events that encode a path from the rat's current location to the HOME well shortly before the rat navigates to HOME following a strikingly similar path. The episode occurred during the first 19 trials, when the specific RANDOM-HOME combinations were novel. (MOV 1214 kb)

Representative episodes consisting of both exploratory behaviour and trajectory events

As video 3, for a second representative episode, also from within the first 19 trials. (MOV 730 kb)

Representative episodes consisting of both exploratory behaviour and trajectory events

As video 3, for a third representative episode, also from within the first 19 trials. (MOV 1373 kb)

Representative episodes consisting of both exploratory behaviour and trajectory events

As video 3, for a fourth representative episode, also from within the first 19 trials. (MOV 1608 kb)

Representative episodes consisting of both exploratory behaviour and trajectory events

As video 3, for a fifth representative episode, also from within the first 19 trials. (MOV 1184 kb)

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Pfeiffer, B., Foster, D. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74–79 (2013). https://doi.org/10.1038/nature12112

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