Vestibular information is required for dead reckoning in the rat

Abstract

Dead reckoning is an on-line form of spatial navigation used by an animal to identify its present location and return directly to a starting location, even after circuitous outward trips. At present, it is not known which of several self-movement cues (efferent copy from movement commands, proprioceptive information, sensory flow, or vestibular information) are used to compute homeward trajectories. To determine whether vestibular information is important for dead reckoning, the impact of chemical labyrinthectomy was evaluated in a test that demanded on-line computation of a homeward trajectory. Rats were habituated to leave a refuge that was visible from all locations on a circular table to forage for large food pellets, which they carried back to the refuge to eat. Two different probe trials were given: (1) the rats foraged from the same spatial location from a hidden refuge in the light and so were able to use visual cues to navigate; (2) the same procedure took place in the dark, constraining the animals to dead reckon. Although control rats carried food directly and rapidly back to the refuge on both probes, the rats with vestibular lesions were able to do so on the hidden refuge but not on the dark probe. The scores of vestibular reflex tests predicted the dead reckoning deficit. The vestibular animals were also impaired in learning a new piloting task. This is the first unambiguous demonstration that vestibular information is used in dead reckoning and also contributes to piloting.

Fig. 1.

Test room and test procedures. Top, The test room. Many visual cues are available to the rat under light conditions; in the dark, visual cues are eliminated. A, Schematic of the table and a possible sequence of food pellet placements for 1 d. Black square indicates cued home base. Rats were required to find each food pellet before the table was rebaited. B, C, Schematics of the place probe–light and place probe–dark. Black circleindicates hidden home base. D, Schematic of the place probe–new location. Gray circle indicates former location of the home base; black circle indicates new location of the home base. For all task components, the heading direction circle that is drawn tangent to the inner portion of the holes was used to code when a return trip was terminated, and the point at which the rat crossed the circle was used to calculate the rat's heading direction.

Fig. 2.

Homeward paths of control and vestibular rats. Each diagram plots the normalized homeward paths for a group of animals under one of the testing conditions: A, homeward paths with the home base cued (black square);B, homeward paths with the home base hidden (black circle); C, homeward paths in the dark. Note: Accuracy with respect to heading direction at the point where rats crossed the heading direction circle is shown in Figure3.

Fig. 3.

Circular statistics for control and vestibular animals illustrating the poor performance of vestibular animals in the dark test. The three testing conditions are as follows:A, training with the home base cue; B, place probe with the home base hidden; C, place probe in the dark. White dots represent control animals;black dots represent vestibular animals. Inner circle represents raw data; outer circlerepresents averaged data. White arrows point to control average heading direction and parameter of concentration. Black arrows point to vestibular average heading direction and parameter of concentration. The bottom of the circular plot corresponds to normalized location of the home base, with heading direction angles increasing from 0 to 360^o in a counterclockwise direction. The length of the arrow corresponds to the group's parameter of concentration, whereas the direction of thearrow represents the group's average heading direction. An arrow that extends to the perimeter of the inner circle represents a parameter of concentration equal to 1, withshorter arrows corresponding to lower values. Note: Only the vestibular animals are inaccurate under the dark condition.

Fig. 4.

Representative control and vestibular animals' kinematic profiles. Outward paths are shown by solid lines; homeward paths are shown by the dotted line in both the representation of the rat's trip (circle) and its speed (graph). The three testing conditions are as follows: A, training with the home base cued; B, place probe with the home base hidden; C, place probe in the dark. Note: The vestibular animal's return trips are only longer and more nondirect in the dark condition.

Fig. 5.

Exploratory trip distance and time (mean and SE). The left-hand panels plot control and vestibular average time (top) and distance (bottom) for the outward trip segment. The right-hand panels plot control and vestibular average time (top) and distance (bottom) for the homeward trip segment (*p <0.05; LSD test). Note: Elevated time and distance in the vestibular rats in the dark.

Fig. 6.

Number of returns (mean and SE) to the old home base location for control and vestibular groups on 2 d of testing with the home base in a new location (*p <0.05; LSD test).

Fig. 7.

Group hole visits when released from a new home base location. A, Location of the first hole selected.B, Location of the second hole selected. Each plot is a diagram of the table with the correct location of the home base, previous location of the home base, and other home base locations indicated by black, gray, andwhite circles, respectively. Hole visits are represented by the black dots located around the outside of the circular diagram. The black arrows indicate average heading direction and parameter of concentration. The length and direction of the black arrow at thecenter of each graph corresponds to a group's parameter of concentration and average heading direction, respectively. Ther values and associated probabilities reflect the results of each plot from the Rayleigh test of randomness.

Fig. 8.

Regression analyses using vestibular reflex impairments as a predictor of spatial performance. White dots represent control animals; black dotsrepresent vestibular animals. The four testing conditions are as follows: A, training with the home base cued;B, place probe with the home base hidden;C, place probe in the dark; D, place probe with the hidden home base in a new location. Spatial performance in A–C was indexed by the parameter of concentration (i.e., variability of heading direction). Spatial performance in D was indexed by mean number of perseverations to the old home base location.