NMDA lesions of Ammon's horn and the dentate gyrus disrupt the direct and temporally paced homing displayed by rats exploring a novel environment: evidence for a role of the hippocampus in dead reckoning

Abstract

Dead reckoning, a form of navigation used to locate a present position and to return to a starting position, is used by rats to return to their home base. The present experiment examined whether dead reckoning is displayed by rats during their first exploratory excursions in a novel environment and also examined whether the behaviour requires the integrity of the cells of the hippocampus. Experimental rats, those with NMDA (N-methyl d-aspartate) lesions of Ammon's horn and the dentate gyrus, and control rats could leave a cage to explore a large circular table under light and dark conditions. Home base behaviour, use of olfactory cues, and thigmotaxic- based navigation were evaluated. Temporal, topographical and kinematic analyses were conducted on the first three exploratory excursions that extended at least halfway across the table. Groups did not differ in numbers of exits from the home base, lingering near the home base, distance travelled, or the use of surface cues as might be exemplified by thigmotaxic and olfactory behaviour. Temporal, topographical and kinematic reconstructions of homing behaviour, however, indicated that control rats, but not hippocampal rats, made direct high velocity return trips to the home base in both the light and the dark. Peak velocity of the trips occurred at the trip midpoint, independent of trip distance, suggesting the movements were preplanned. These results are discussed in relation to the ideas that dead reckoning is used in the homing of exploring rats and that this form of navigation involves the hippocampus.

Movements of exploration intact in rats with hippocampal lesions

“…There was only slight damage to the overlying corpus callosum and cortex at the sites of cannula penetration. The lesion extent is consistent with previous studies involving selective hippocampal damage [22,44]. Photomicrographs from three rostral-caudal levels from a rat with a NMDA (N-methyl d-aspartate) injection into the hippocampus (left) and from a control rat (right).…”

“…In an exploratory test situation very similar to that used in the present study, except that the rats were provided with a refuge box from which to explore, no differences in activity were observed over a number of test days in control versus hippocampal rats because neither group made many excursions from the refuge [44]. Thus, it is not clear whether rats in "exploratory" tests situations, such as that described here, are exploring as opposed to attempting to find an exit from the test situation.…”

“…One hippocampal animal also failed to engage in any locomotor activity in any test situation, and rather remained close to the proximal cue. It is possible that for this animal the cue was so dominant as to suppress locomotor activity, as occurs when an animal is given a refuge [44]. Future research could examine the significance of the salience of ambient cues to control and hippocampal rats.…”

“…1) was a wooden circular table without walls measuring 255 cm in diameter [44]. The absence of walls reduced the probability that the rats would display thigmotaxic behavior to the edge of the open field.…”

“…We used a test situation that is conducive for eliciting both home base behavior and excursions [2,16,17]. To produce selective lesions of the hippocampus, injections of the neurotoxin Nmethyl d-aspartate (NMDA) were made into the cell fields of Ammon's horn and the dentate gyrus [22,44]. After a recovery period, control rats and rats with hippocampal lesions were placed on a circular table-top under lighted conditions on each of four daily sessions.…”