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Path integration: how the head direction signal maintains and corrects spatial orientation

Abstract

Head-direction cells have frequently been regarded as an internal 'compass' that can be used for navigation, although there is little evidence showing a link between their activity and spatial behavior. In a navigational task requiring the use of internal cues to return to a home location without vision (path integration), we found a robust correlation between head-direction cell activity and the rat's heading error in the rat's homing behavior. We observed two different correction processes that rats used to improve performance after an error. The more frequent one consists of 'resetting' the cell whenever the rat returns to the home location. However, we found that when large errors occur, the head-direction system has the ability to 'remap' and set a new reference frame, which is then used in subsequent trials. We also offer some insight into how these two correction processes operate when rats make an error.

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Figure 1: Head-direction cell and behavioral procedure.
Figure 2: Hypothesized relationship between the PFD shift and the rat's heading error.
Figure 3: Examples of the foraging path with the corresponding tuning curve of a head-direction cell recorded during that trial.
Figure 4: Variations of the PFD in the refuge.
Figure 5: The correction process.
Figure 6: Examples of remapping and resetting sessions.
Figure 7: Moment-to-moment changes of the cell's PFD in two examples of resetting trials.
Figure 8: Moment-to-moment changes of the cell's PFD in an example of a remapping trial.

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Acknowledgements

We thank R. Leaton, P. Trifieff and E. Lesburgueres for their valuable comments on the manuscript. These experiments were supported by US National Institutes of Health grants DC009318 and NS053907.

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S.V. and J.S.T. conceived and designed the study, discussed the findings, and wrote the manuscript. S.V. performed the experiments and analyzed the results.

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Correspondence to Jeffrey S Taube.

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The authors declare no competing financial interests.

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Valerio, S., Taube, J. Path integration: how the head direction signal maintains and corrects spatial orientation. Nat Neurosci 15, 1445–1453 (2012). https://doi.org/10.1038/nn.3215

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