Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

References

  1. Darwin, C. Origin of certain instincts. Nature VII, 417–418 (1873).

    Article  Google Scholar 

  2. Mittelstaedt, M.L. & Mittelstaedt, H. Homing by path integration in a mammal. Naturwissenschaft 67, 566–567 (1980).

    Article  Google Scholar 

  3. Etienne, A.S. & Jeffery, K.J. Path integration in mammals. Hippocampus 14, 180–192 (2004).

    Article  Google Scholar 

  4. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).

    Article  CAS  Google Scholar 

  5. Taube, J.S., Muller, R.U. & Ranck, J.B. Head-direction cells recorded from the postsubiculum of freely-moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435 (1990).

    Article  CAS  Google Scholar 

  6. Hafting, T., Fyhn, M., Molden, S., Moser, M.B. & Moser, E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).

    Article  CAS  Google Scholar 

  7. Muir, G.M. & Taube, J.S. The neural correlates of navigation: do head direction and place cells guide spatial behavior? Behav. Cogn. Neurosci. Rev. 1, 297–317 (2002).

    Article  Google Scholar 

  8. Save, E. & Poucet, B. Do place cells guide spatial behaviour? in Hippocampal Place fields, Relevance to learning and memory (ed., Mizumori, S.J.) 138–149 (Oxford University Press, New York, 2008).

  9. Wiener, S.I. & Taube, J.S. (eds.). Head Direction Cells and the Neural Mechanisms of Spatial Orientation (MIT Press, Cambridge, Massachusetts, USA, 2005).

  10. Taube, J.S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181–207 (2007).

    Article  CAS  Google Scholar 

  11. McNaughton, B.L., Chen, L.L. & Markus, E.J. “Dead reckoning”, landmark learning, and the sense of direction: a neurphysiological and computational hypothesis. J. Cogn. Neurosci. 3, 190–202 (1991).

    Article  CAS  Google Scholar 

  12. Taube, J.S. Head direction cells and the neurophysiological basis for a sense of direction. Prog. Neurobiol. 55, 225–256 (1998).

    Article  CAS  Google Scholar 

  13. van der Meer, M.A., Richmond, Z., Braga, R.M., Wood, E.R. & Dudchenko, P.A. Evidence for the use of an internal sense of direction in homing. Behav. Neurosci. 124, 164–169 (2010).

    Article  Google Scholar 

  14. McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I. & Moser, M.B. Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663–678 (2006).

    Article  CAS  Google Scholar 

  15. Hasselmo, M.E. Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18, 1213–1229 (2008).

    Article  Google Scholar 

  16. Gallistel, C.R. The organization of learning (MIT Press, Cambridge, Massachusetts, USA, 1990).

  17. Souman, J.L., Frissen, I., Sreenivasa, M.N. & Ernst, M.O. Walking straight into circles. Curr. Biol. 19, 1538–1542 (2009).

    Article  CAS  Google Scholar 

  18. Etienne, A.S., Maurer, R., Boulens, V., Levy, A. & Rowe, T. Resetting the path integrator: a basic condition for route-based navigation. J. Exp. Biol. 207, 1491–1508 (2004).

    Article  Google Scholar 

  19. Knaden, M. & Wehner, R. Ant navigation: resetting the path integrator. J. Exp. Biol. 209, 26–31 (2006).

    Article  Google Scholar 

  20. Taube, J.S. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15, 70–86 (1995).

    Article  CAS  Google Scholar 

  21. Whishaw, I.Q., Coles, B.L. & Bellerive, C.H. Food carrying: a new method for naturalistic studies of spontaneous and forced alternation. J. Neurosci. Methods 61, 139–143 (1995).

    Article  CAS  Google Scholar 

  22. Etienne, A.S., Boulens, V., Maurer, R., Rowe, T. & Siegrist, C. A brief view of known landmarks reorientates path integration in hamsters. Naturwissenschaften 87, 494–498 (2000).

    Article  CAS  Google Scholar 

  23. Goodridge, J.P. & Taube, J.S. Preferential use of the landmark navigational system by head direction cells in rats. Behav. Neurosci. 109, 49–61 (1995).

    Article  CAS  Google Scholar 

  24. Goodridge, J.P., Dudchenko, P.A., Worboys, K.A., Golob, E.J. & Taube, J.S. Cue control and head direction cells. Behav. Neurosci. 112, 749–761 (1998).

    Article  CAS  Google Scholar 

  25. Clark, B.J., Harris, M.J. & Taube, J.S. Control of anterodorsal thalamic head direction cells by environmental boundaries: Comparison with conflicting distal landmarks. Hippocampus 22, 172–187 (2012).

    Article  Google Scholar 

  26. Golob, E.J., Stackman, R.W., Wong, A.C. & Taube, J.S. On the behavioral significance of head direction cells: neural and behavioral dynamics during spatial memory tasks. Behav. Neurosci. 115, 285–304 (2001).

    Article  CAS  Google Scholar 

  27. Cheng, K. Whither geometry? Troubles of the geometric module. Trends Cogn. Sci. 12, 355–361 (2008).

    Article  Google Scholar 

  28. Steck, K., Hansson, B.S. & Knaden, M. Desert ants benefit from combining visual and olfactory landmarks. J. Exp. Biol. 214, 1307–1312 (2011).

    Article  Google Scholar 

  29. Collett, T.S. & Graham, P. Animal navigation: path integration, visual landmarks and cognitive maps. Curr. Biol. 14, R475–R477 (2004).

    Article  CAS  Google Scholar 

  30. Gothard, K.M., Skaggs, W.E. & McNaughton, B.L. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci. 16, 8027–8040 (1996).

    Article  CAS  Google Scholar 

  31. Gothard, K.M., Skaggs, W.E., Moore, K.M. & McNaughton, B.L. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J. Neurosci. 16, 823–835 (1996).

    Article  CAS  Google Scholar 

  32. Derdikman, D. et al. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 12, 1325–1332 (2009).

    Article  CAS  Google Scholar 

  33. Taube, J.S., Muller, R.U. & Ranck, J.B. Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10, 436–447 (1990).

    Article  CAS  Google Scholar 

  34. Muller, R.U. & Kubie, J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951–1968 (1987).

    Article  CAS  Google Scholar 

  35. Markus, E.J. et al. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. 15, 7079–7094 (1995).

    Article  CAS  Google Scholar 

  36. Leutgeb, S. et al. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309, 619–623 (2005).

    Article  CAS  Google Scholar 

  37. Knierim, J.J., Kudrimoti, H.S. & McNaughton, B.L. Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J. Neurophysiol. 80, 425–446 (1998).

    Article  CAS  Google Scholar 

  38. Knierim, J.J., Kudrimoti, H.S. & McNaughton, B.L. Place cells, head direction cells, and the learning of landmark stability. J. Neurosci. 15, 1648–1659 (1995).

    Article  CAS  Google Scholar 

  39. Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473–500 (2000).

    Article  CAS  Google Scholar 

  40. Fiorillo, C.D., Tobler, P.N. & Schultz, W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299, 1898–1902 (2003).

    Article  CAS  Google Scholar 

  41. Sharp, P.E., Tinkelman, A. & Cho, J. Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of gudden in the rat: implications for path integration in the head direction cell circuit. Behav. Neurosci. 115, 571–588 (2001).

    Article  CAS  Google Scholar 

  42. Bassett, J.P. & Taube, J.S. Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J. Neurosci. 21, 5740–5751 (2001).

    Article  CAS  Google Scholar 

  43. Matsumoto, M. & Hikosaka, O. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447, 1111–1115 (2007).

    Article  CAS  Google Scholar 

  44. Balcita-Pedicino, J.J., Omelchenko, N., Bell, R. & Sesack, S.R. The inhibitory influence of the lateral habenula on midbrain dopamine cells: ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus. J. Comp. Neurol. 519, 1143–1164 (2011).

    Article  CAS  Google Scholar 

  45. Ito, S., Stuphorn, V., Brown, J.W. & Schall, J.D. Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302, 120–122 (2003).

    Article  CAS  Google Scholar 

  46. Michelet, T., Bioulac, B., Guehl, D., Goillandeau, M. & Burbaud, P. Single medial prefrontal neurons cope with error. PLoS ONE 4, e6240 (2009).

    Article  Google Scholar 

  47. Whishaw, I.Q., Maaswinkel, H., Gonzalez, C.L. & Kolb, B. Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions. Behav. Brain Res. 118, 67–76 (2001).

    Article  CAS  Google Scholar 

  48. Bouret, S. & Sara, S.J. Network reset: a simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 28, 574–582 (2005).

    Article  CAS  Google Scholar 

  49. Frohardt, R.J., Bassett, J.P. & Taube, J.S. Path integration and lesions within the head direction cell circuit: comparison between the roles of the anterodorsal thalamus and dorsal tegmental nucleus. Behav. Neurosci. 120, 135–149 (2006).

    Article  Google Scholar 

  50. Whishaw, I.Q. & Maaswinkel, H. Rats with fimbria-fornix lesions are impaired in path integration: a role for the hippocampus in “sense of direction”. J. Neurosci. 18, 3050–3058 (1998).

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Jeffrey S Taube.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–16 (PDF 4436 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3215

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing