Evidence for the Use of an Internal Sense of Direction in Homing Matthijs A. A. van der Meer, Zoe Richmond, Rodrigo M. Braga, and Emma R. Wood University of Edinburgh Paul A. Dudchenko University of Edinburgh and Stirling University Path integration, the ability to maintain a representation of location and direction on the basis of internal cues, is thought to be important for navigation and the learning of spatial relationships. Representations of location and direction in the brain, such as head direction cells, grid cells, and place cells in the limbic system, are thought to underlie navigation by path integration. While this idea is generally consistent with lesion studies, the relationship between such neural activity and behavior has not been studied on a task where animals demonstrably use a path integration strategy. Here we report the development of such a task in rats: by slowly rotating rats before their return to a trial-unique home base, we could show subjects relied on internal cues only to navigate. To illustrate how this task can be combined with recording, we show examples of simultaneously recorded head direction cells in which neural activity is closely related to rats’ homing direction. These results support the notion that rats can navigate by path integration, that this ability depends on head direction cells, and suggest a convenient behavioral paradigm for investi- gating the neural basis of navigation. Keywords: path integration, head direction, navigation, rat Supplemental materials: http://dx.doi.org/10.1037/a0018446.supp Navigation is an important survival skill for many mammals, such as for rats returning to their nest after a foraging trip, or for humans attempting to find their car in the parking lot. A major subdivision between navigation strategies is that between those relying on external cues, such as landmarks in the environment, and those relying on internal cues, such as vestibular or proprio- ceptive feedback (O’Keefe and Nadel, 1978; Scho ¨ne, 1984; Gal- listel, 1990; Redish, 1999). The latter strategy is referred to as “dead reckoning” or path integration, and is thought to be impor- tant, not only when external cues are unavailable or unreliable, but also for learning spatial relationships, such as the construction of “cognitive maps” (McNaughton, Battaglia, Jensen, Moser, & Moser, 2006). Demonstrating path integration experimentally can be difficult because of the variety of potential external-cue-based alternative strategies that need to be ruled out (Jeffery & Etienne, 2004). In rodents, a number of tasks have been developed that encourage a path integration strategy by attempting to minimize the availability or informativeness of external cues (e.g., Etienne, Maurer, Saucy, & Teroni, 1986; Whishaw & Tomie, 1997; Pearce, Roberts, & Good, 1998); the fact that subjects typically still do well in such tasks (although usually not as well compared to when landmarks are available) supports the notion that they are unlikely to be relying on external cues. A complementary approach has been to analyze subtle aspects of navigation behavior, such as structural biases in homing (suggesting path integration errors, Se ´guinot, Maurer, & Etienne, 1993) or detailed speed profiles (suggesting rats know the distance to a home box even on their first outbound journey, Wallace & Whishaw, 2003). Taken to- gether, these results support the idea that rodents can navigate on the basis of internal cues alone. However, the neural basis of path integration remains the sub- ject of debate. Theoretically, a combination of direction and dis- tance information is sufficient to plan a direct path between any two points, leading to the proposal that “head direction cells” (Taube, 2007), and “place cells” or “grid cells” (Moser, Kropff, & Moser, 2008) in the limbic system might support path integration (McNaughton, Chen, & Markus, 1991). While this notion has generally been supported by lesion studies (e.g., Wallace & Whishaw, 2003; Wilton, Baird, Muir, Honey, & Aggleton, 2001; Vann, 2005; Frohardt, Bassett, & Taube, 2006; but see Alyan & McNaughton, 1999; Shrager, Kirwan, & Squire, 2008), attempts to relate neural activity to spatial behavior have yielded contradictory results (Golob, Stackman, Wong, & Taube, 2001; Muir & Taube, 2004; Jeffery, Gilbert, Burton, & Strudwick, 2003; Lenck-Santini, Muller, Save, & Poucet, 2002). A limitation of these studies is that they do not provide evidence that rats are in fact path integrating, raising the possibility that they are solving tasks by strategies that Matthijs A. A. van der Meer, Centre for Cognitive and Neural Systems, Neuroinformatics Doctoral Training Centre, University of Edinburgh, Ed- inburgh, U.K.; Zoe Richmond, Rodrigo M. Braga, and Emma R. Wood, Centre for Cognitive and Neural Systems, University of Edinburgh, Edin- burgh, U.K.; and Paul A. Dudchenko, Centre for Cognitive and Neural Systems, University of Edinburgh, Edinburgh, U.K., and Department of Psychology, Stirling University, Stirling, U.K. Supported by an EPSRC/MRC Neuroinformatics Doctoral Training Centre studentship to MvdM. We thank Hugh Cameron, Douglas Howie, and Robert MacGregor for apparatus design and construction, Kate Shires for help with running animals, Rosamund Langston and James Ainge for assistance with surgery, Jane Tulloch for histology, and Neil Burgess, Mayank Dutia, A. David Redish, and Mark van Rossum for discussion. This work has been previously published in abstract form (Society for Neuroscience annual meeting, 2007). Correspondence concerning this article should be addressed to Matthijs A. A. van der Meer, Department of Neuroscience, University of Minnesota, 6-145 Jackson Hall, 321 Church St. SE, Minneapolis, MN 55455. E-mail: mvdm@umn.edu Behavioral Neuroscience © 2010 American Psychological Association 2010, Vol. 124, No. 1, 164 –169 0735-7044/10/$12.00 DOI: 10.1037/a0018446 164 This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.