Otoconia‐deficient mice show selective spatial deficits

Abstract

Damage or inactivation of the vestibular system impairs performance on various spatial memory tasks, but few studies have attempted to disambiguate the roles of the semicircular canals and otolith organs in this performance. The present study tested the otolithic contribution to spatial working and reference memory by evaluating the performance of otoconia-deficient tilted mice on a radial arm maze and a Barnes maze. One radial arm maze task provided both intramaze and extramaze cues, whereas the other task provided only extramaze cues. The Barnes maze task provided only extramaze cues. On the radial arm maze, tilted mice performed similar to control mice when intramaze cues were available, but made more working and reference memory errors than control mice when only extramaze cues were available. On the Barnes maze task, control and tilted mice showed similar latency, distance, and errors during acquisition training. On the subsequent probe trial, both groups spent the greatest percentage of time in the goal quadrant, indicating they were able to use extramaze cues to guide their search. Overall, these results suggest signals originating in the otolith organs contribute to spatial memory, but are not necessary for all aspects of spatial performance.

Otolith dysfunction alters exploratory movement in mice

“…In fact, rats with complete vestibular lesions were able to perform relatively well on the homing task in light [18], despite the fact that vestibular lesions or inactivation completely abolishes the head direction signal [13, 14]. However, tilted mice were impaired at performing a radial arm maze discrimination task in light when only distal cues were available to guide navigation [23]. Thus, signals from the otolith organs have an important role in the directional aspect of navigation, and visual information can compensate for these deficits in some tasks.…”

“…The otolith organs also contribute to head direction cell function, but this contribution appears to be relatively less than that of the canals; otoconia-deficient mice have head direction cells that are directionally tuned, but this tuning degrades over time [22]. Nevertheless, the degraded head direction signal of otoconia-deficient mice is paralleled by deficits in the performance of directional navigation tasks such as the radial arm maze, food-carrying (homing) task, and Y-maze alternation [4, 23, 24] for review, see [25]. However, otoconia-deficient mice were able to accurately perceive the goal location during the probe trial on a Barnes maze, suggesting place recognition was intact [23].…”

“…Nevertheless, the degraded head direction signal of otoconia-deficient mice is paralleled by deficits in the performance of directional navigation tasks such as the radial arm maze, food-carrying (homing) task, and Y-maze alternation [4, 23, 24] for review, see [25]. However, otoconia-deficient mice were able to accurately perceive the goal location during the probe trial on a Barnes maze, suggesting place recognition was intact [23]. The available evidence thus suggests that otolith signals contribute heavily to the directional aspect of navigation in both visual and non-visual environments, but have a lesser role in the locational aspect.…”

Linear Self-Motion Cues Support the Spatial Distribution and Stability of Hippocampal Place Cells

“…Because head direction cell activity and landmark navigation is known to be disrupted in tilted mice, [7,9] we assessed landmark control over place cell activity by rotating the cue card in session 2 and measuring the degree to which place cells were anchored to that cue.…”

“…Otoconia-deficient head tilt mice are known to have attenuated vestibulo-ocular reflex [23], and this deficit may be present in tilted mice. However, previous studies show that tilted mice are able to rely on their visual system to navigate to cues, and their performance suffers to a greater extent in non-visual environments or when visual cues are sparse [9,24,25]. …”