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Multiplexed code of navigation variables in anterior limbic areas

The brain’s navigation system integrates multimodal cues to create a sense of position and orientation. Here we used a multimodal model to systematically assess how neurons in the anterior thalamic nuclei, retrosplenial cortex and anterior hippocampus of mice, as well as in the cingulum fiber bundle and the white matter regions surrounding the hippocampus, encode an array of navigational variables when animals forage in a circular arena. In addition to coding head direction, we found that some thalamic cells encode the animal’s allocentric position, similar to place cells. We also found that a large fraction of retrosplenial neurons, as well as some hippocampal neurons, encode the egocentric position of the arena’s boundary. We compared the multimodal model to traditional methods of head direction tuning and place field analysis, and found that the latter were inapplicable to multimodal regions such as the anterior thalamus and retrosplenial cortex. Our results draw a new picture of the signals carried and outputted by the anterior thalamus and retrosplenial cortex, offer new insights on navigational variables represented in the hippocampus and its vicinity, and emphasize the importance of using multimodal models to investigate neural coding throughout the navigation system.