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Multisensory Control of Hippocampal Spatiotemporal Selectivity

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Science  14 Jun 2013:
Vol. 340, Issue 6138, pp. 1342-1346
DOI: 10.1126/science.1232655

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A Sense of Place

Hippocampal place cells are believed to be mainly governed by visual and self-motion cues. However, the contribution of sensory cues such as smells, sounds, and textures, etc., is difficult to eliminate. In virtual reality, these cues will not provide any information about the animals' position. Ravassard et al. (p. 1342, published online 2 May) developed a virtual-reality system as immersive and close to the real world as possible and compared place cells in rats running in this apparatus and in the real world. Twice as many neurons were active in a real-world situation compared to virtual reality. While place cells in the real world encoded position, place cells in a virtual world encoded distance.

Abstract

The hippocampal cognitive map is thought to be driven by distal visual cues and self-motion cues. However, other sensory cues also influence place cells. Hence, we measured rat hippocampal activity in virtual reality (VR), where only distal visual and nonvestibular self-motion cues provided spatial information, and in the real world (RW). In VR, place cells showed robust spatial selectivity; however, only 20% were track active, compared with 45% in the RW. This indicates that distal visual and nonvestibular self-motion cues are sufficient to provide selectivity, but vestibular and other sensory cues present in RW are necessary to fully activate the place-cell population. In addition, bidirectional cells preferentially encoded distance along the track in VR, while encoding absolute position in RW. Taken together, these results suggest the differential contributions of these sensory cues in shaping the hippocampal population code. Theta frequency was reduced, and its speed dependence was abolished in VR, but phase precession was unaffected, constraining mechanisms governing both hippocampal theta oscillations and temporal coding. These results reveal cooperative and competitive interactions between sensory cues for control over hippocampal spatiotemporal selectivity and theta rhythm.

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