Navigation and the underlying brain signals are influenced by various allothetic and idiothetic cues, depending on environmental conditions and task demands. Visual landmarks typically control navigation in familiar environments but, in the absence of landmarks, self-movement cues are able to guide navigation relatively accurately. These self-movement cues include signals from the vestibular system, and may originate in the semicircular canals or otolith organs. Here, we tested the otolithic contribution to navigation on a food-hoarding task in darkness and in light. The dark test prevented the use of visual cues and thus favored the use of self-movement information, whereas the light test allowed the use of both visual and non-visual cues. In darkness, tilted mice made shorter-duration stops during the outward journey, and made more circuitous homeward journeys than control mice; heading error, trip duration, and peak error were greater for tilted mice than for controls. In light, tilted mice also showed more circuitous homeward trips, but appeared to correct for errors during the journey; heading error, trip duration, and peak error were similar between groups. These results suggest that signals from the otolith organs are necessary for accurate homing performance in mice, with the greatest contribution in non-visual environments.

The organization of rodent exploratory behavior appears to depend on self-movement cue processing. As of yet, however, no studies have directly examined the vestibular system’s contribution to the organization of exploratory movement. The current study sequentially segmented open field behavior into progressions and stops in order to characterize differences in movement organization between control and otoconia-deficient tilted mice under conditions with and without access to visual cues. Under completely dark conditions, tilted mice exhibited similar distance traveled and stop times overall, but had significantly more circuitous progressions, larger changes in heading between progressions, and less stable clustering of home bases, relative to control mice. In light conditions, control and tilted mice were similar on all measures except for the change in heading between progressions. This pattern of results is consistent with otoconia-deficient tilted mice using visual cues to compensate for impaired self-movement cue processing. This work provides the first empirical evidence that signals from the otolithic organs mediate the organization of exploratory behavior, based on a novel assessment of spatial orientation.

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Spatial and temporal information processing provide a foundation for higher cognitive functions. The survival of animals depends on integrating spatial and temporal information to organize behavior. In general, previous research has focused on only one source of information processing; however, there is evidence to support a convergence in the processing of egocentric-spatial and temporal information within a cortico-striatal system of structures. The current study evaluated the contributions of the dorsocentral striatum (DCS) to egocentric-spatial and temporal (within the seconds-to-minutes range) processing of information using a food protection task. Long-Evans rats received unilateral NMDA lesions of the DCS followed by testing in a food protection task. Performance in this task is mediated by the motivation of the animal to consume a food item, their perception of the time required to consume a food item, their sensory ability to process egocentric cues, and their motor ability to evade an incoming conspecific. Unilateral DCS lesions were shown to impact both spatial and temporal characteristics of food protection. These results suggest that the DCS may be a critical structure for the integration of egocentric-spatial and temporal information within the interval timing range.

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