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.

Path integration in mammals

“…Contradicting these results, however, are findings reported by Alyan and McNaughton (1999) of intact PI in hippocampectomized animals, a discrepancy that has not yet been explained. Further supporting a PI role for the hippocampus, hippocampal lesions impair angular PI by head direction cells (Golob and Taube, 1999) and vestibular lesions, which disrupt the place cell representation (Taube et al, 1996), also impair path integration (Cohen, 2000;Wallace et al, 2002).…”

“…Recent studies have indicated an important role for the vestibular system in path integration, as animals and humans with vestibular damage show navigational impairment in the absence of landmarks (Cohen, 2000;Slackman et al, 2002;Wallace et al, 2002). Other types of information may play a part as well, such as short-term copies of locomotor commands (efference copies) and inertial signals due to acceleration from extravestibular gravity receptors (Mittelstaedt, 1999; for review, see Berthoz et al, 1999;Etienne et al, 1996).…”

The development of spatial capacity in piloting and dead reckoning by infant rats: Use of the huddle as a home base for spatial navigation

“…Although it is possible that in the early postnatal period the short returns of rat pups are guided by local cues, for longer trips at older ages it is likely that the pups are using dead reckoning, as has been suggested for adult rats (Wallace et al, 2002a(Wallace et al, ,b, 2003Whishaw & Gorny 1999;Whishaw, Hines, & Wallace, 2001). First, direct returns persisted in infra red light, in which visual cues cannot be seen.…”

“…Previous studies with adult rats have found that exploration is organized, and consists of two component spatial behaviors, piloting and dead reckoning (Wallace et al, 2002a(Wallace et al, ,b, 2003. If rats are provided with a home base in an otherwise open arena, they use the base as a center for their exploratory behavior.…”

“…Exploratory behavior was divided into the following components, using previously defined categories (Wallace et al, 2002a(Wallace et al, ,b, 2003:…”