Otolithic information is required for homing in the mouse

Abstract

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.

Keywords: head direction; navigation; path integration; self-movement; vestibular.

Figure 1

Kinematic (left) and topographic (top) characteristics are plotted for a representative control (top) and tilted mouse (bottom) on the homing task in darkness. The outward path (gray line) is circuitous for both mice; the homeward segment (black line) is relatively direct for the control mouse, but is more circuitous for the tilted mouse.

Figure 2

Kinematic characteristics are plotted for control and tilted mice in darkness. A, Tilted mice (TILT) completed the outward segment faster than control mice (CON). However, tilted mice took longer to complete the homeward segment than control mice. B, Tilted mice’s faster performance of the outward segment did not result from fewer stops per trip. C, However, the duration of stops was shorter for tilted mice than for control mice. D, Peak speed did not differ between groups for either trip segment. *p < .05 Mean ± SEM.

Figure 3

Topographic characteristics are plotted for control and tilted mice in darkness. A, The outward segment was circuitous for both groups of mice. Upon finding the food, control (CON) mice returned relatively directly to the refuge, whereas tilted (TILT) mice took a more circuitous route. B, Tilted mice showed greater heading error than control mice. C, Peak speed occurred at a greater distance from the mid-point for tilted mice than for control mice. *p < .05 Mean ± SEM.

Figure 4

Kinematic (left) and topographic (top) characteristics are plotted for a representative control (top) and tilted mouse (bottom) on the homing task in light. The outward path (gray line) is circuitous for both mice, whereas the homeward segment (black line) is relatively direct for both mice.

Figure 5

Kinematic characteristics of control and tilted mice in light. A, Both control (CON) and tilted mice (TILT) completed the homeward segment faster than the outward segment. Groups did not differ on segment duration. B, Control and tilted mice showed similar numbers of stops per trip, and C, the duration of stops was similar between groups. D, Peak speed did not differ between groups for either trip segment. Mean ± SEM.

Figure 6

Topographic characteristics are plotted for control and tilted mice under light conditions. A, The outward segment was relatively circuitous for both groups of mice. Upon finding the food, control (CON) mice returned relatively directly to the refuge, whereas tilted (TILT) mice took a slightly more circuitous route. B, Both groups showed similar heading error during the homeward segment. C, Peak speed occurred relatively close to the mid-point of the homeward segment for both groups. *p < .05 Mean ± SEM.