Otolith dysfunction alters exploratory movement in mice

Abstract

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.

Keywords: Compensation; Dead reckoning; Open field behavior; Path integration; Sequential analysis; Vestibular system.

Figure 1

Circular panels plot paths (black line) followed by a representative control (A, B, C, D) and tilted (E, F, G, H) mice during each sample under dark conditions. Each group’s average total distance traveled (panel I) and stop time (panel J) are plotted for the four five-minute samples under dark conditions.

Figure 2

Circular panels plot the path (black line) and progression Euclidean distances (grey lines) for the same representative control (A, B, C, D) and tilted (E, F, G, H) mice under dark conditions. Each group’s average progression peak speed (I), distance (J), and path circuity (K) are plotted for the four five-minute samples under dark conditions.

Figure 3

Circular panels plot the path (black line) and stop location (grey circles) with diameter representing relative stop duration for the same representative control (A, B, C, D) and tilted (E, F, G, H) mice under dark conditions. Each group’s average stop duration (I) and between progression change-in-heading (J) are plotted for the four five-minute samples under dark conditions.

Figure 4

Circular panels plot stop frequencies relative to polar heading direction for the same representative control (A, B, C, D) and tilted (E, F, G, H) mice under dark conditions. Average heading (theta) and parameter of concentration (r) are provided for each sample and represented by the polar line graph originating at the center of each plot. Group average parameter of concentration is plotted for each sample under dark condition (I). Average parameter of concentration (calculated from each mouse’s four average heading directions) is plotted for both groups (J). (*<0.05)

Figure 5

Circular panels plot paths (black line) followed by representative control (A, B, C, D) and tilted (E, F, G, H) mice during each sample under light conditions. Each group’s average total distance traveled (I) and stop time (J) are plotted for the four five-minute samples under light conditions.

Figure 6

Circular panels plot the path (black line) and progression Euclidean distances (grey lines) for the same representative control (A, B, C, D) and tilted (E, F, G, H) mice under light conditions. Each group’s average progression peak speed (I), distance (J), and path circuity (K) is plotted for the four five-minute samples under light conditions.

Figure 7

Circular panels plot the path (black line) and stop location (grey circles) with diameter representing relative stop duration for the same representative control (A, B, C, D) and tilted (E, F, G, H) mice under light conditions. Each group’s average stop duration (I) and between progression change-in-heading (J) are plotted for the four five-minute samples under light conditions.

Figure 8

Circular panels plot stop frequencies relative to polar heading direction for the same representative control (A, B, C, D) and tilted (E, F, G, H) mice under light conditions. Average heading (theta) and parameter of concentration (r) are provided for each sample and represented by the polar line graph originating at the center of each plot. Group average parameter of concentration is plotted for each sample under light conditions (I). Average parameter of concentration (calculated from each mouse’s four average heading directions) is plotted for both groups (J).