Douglas G. Wallace

Dead reckoning (path integration) requires the hippocampal formation: evidence from spontaneous exploration and spatial learning tasks in light (allothetic) and dark (idiothetic) tests

Animals navigate using cues generated by their own movements (self-movement cues or idiothetic cues), as well as the cues they encounter in their environment (distal cues or allothetic cues). Animals use these cues to navigate in two different ways. When dead reckoning (deduced reckoning or path integration), they integrate self-movement cues over time to locate a present position or to return to a starting location. When piloting, they use allothetic cues as beacons, or they use the relational properties of allothetic cues to locate places in space. The neural structures involved in cue use and navigational strategies are still poorly understood, although considerable attention is directed toward the contributions of the hippocampal formation (hippocampus and associated pathways and structures, including the fimbria-fornix and the retrosplenial cortex). In the present study, using tests in allothetic and idiothetic paradigms, we present four lines of evidence to support the hypothesis that the hippocampal formation plays a central role in dead reckoning. (1) Control but not fimbria-fornix lesion rats can return to a novel refuge location in both light and dark (infrared) food carrying tasks. (2). Control but not fimbria-fornix lesion rats make periodic direct high velocity returns to a starting location in both light and dark exploratory tests. Control but not fimbria-fornix rats trained in the light to carry food from a fixed location to a refuge are able to maintain accurate outward and homebound trajectories when tested in the dark. (3). Control but not fimbria-fornix rats are able to correct an outward trajectory to a food source when the food source is moved when allothetic cues are present. These, tests of spontaneous exploration and foraging suggest a role for the hippocampal formation in dead reckoning.

Rats can track odors, other rats, and themselves: implications for the study of spatial behavior.

In order to demonstrate that rats solve dead reckoning (path integration) tasks in which they return to a starting location using self-movement (idiothetic) cues, it is necessary to remove external (allothetic) cues. Odor cues, especially those generated by a rat on a single passage, are difficult to control and they can potentially serve as a cue to guide a homeward trip. Because it is presently unknown whether rats can track the cues that they themselves leave, as opposed to the odor trails left by other rats, we investigated this question in the present study. A tracking task was used in which rats: (1) followed a scented string from a refuge to obtain a food pellet located on a large circular table; (2) followed odors left on the table; (3) followed odors left by the passage of another rat; or (4) followed odors left by themselves. Groups of rats were presented with strings scented with either the rats own odor (Group Own), a conspecifics odor (Group Other), or another scent, vanilla (Group Vanilla). After training, a series of discrimination tests were given to determine the nature of the stimulus that controls scent tracking. The results indicated that Own, Other, and Vanilla groups were equally proficient in discriminating and following their respective odors. The rats were also able to follow odor trails on the table surface as well as a trail left by the single passage of another rat or their own passage. This is the first study to demonstrate that rats can discriminate between conspecific odors and their own odor left during a single passage. The results are discussed in relation to their implications for experimental methodology and olfactory contributions to spatial navigation in general and dead reckoning in particular.

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

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‐methly d‐aspartate) lesions of Ammons 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.

Quantification of a single exploratory trip reveals hippocampal formation mediated dead reckoning

A rats proclivity to explore a novel environment presents a behaviorally rich paradigm to investigate the role of the hippocampus in spatial navigation. Here we describe a novel technique of behavioral analysis that is derived from a single exploratory trip. An exploratory trip was defined as a rats departure from the home base that ended when the rat returned to the home base. The behavior observed on a single exploratory trip by a control animal is highly organized into outward and homeward segments. An outward segment is characterized by a slow circuitous progression from the home base marked by several stops. A homeward segment is characterized by a rapid direct return to the home base. The velocity attribute of the exploratory trip was quantified by estimating the point of inflection associated with the trips cumulative moment-to-moment velocity distribution. The heading direction and variance of the homeward trip segment was analyzed with circular statistics. A comparison of the exploratory behavior of control animals and animals with damage to the fimbria-fornix indicated that the velocity and heading direction of the homeward portion of the trip depends upon the hippocampal formation. While control and fimbria-fornix rats had similar outward segments, the return paths of the fimbria-fornix rats were significantly slower, more circuitous, and more variable compared with that of the control rats. This result was also independent of testing in light or dark conditions. The lack of dependence on allothetic cues suggests that rats employ dead reckoning navigational strategies to initiate the homeward portion of exploratory movements. Methods to quantify exploratory behavior in terms of velocity and angular components provide an assessment of control behavior and the assessment of the behavior of rats with hippocampal formation damage that is easy to implement.

On the origins of autobiographical memory

Tolving argues that one form of explicit memory, autobiographical memory is uniquely human and has no nonhuman animal antecedents. We suggest that a form of memory used by humans and nonhuman animals, dead reckoning, shares a common limbic structure, including the cingulate cortex and hippocampus, and involves similar processes in recognition of self-action. Thus, it may be homologous to, and an antecedent of, autobiographical memory in humans.

Odor tracking in rats with orbital frontal lesions.

Rats track self-, conspecific, and artificial odors to locate food. The orbital frontal cortex has been implicated in olfactory behavior, but whether it plays a role in a species-typical behavior, such as odor-guided navigation, has not been studied. Rats were trained to track 1 of 3 different odors deposited on a string. After rats were reliably tracking a scented string, they received a series of 2- and 3-odor discrimination tests. Next, all the rats received bilateral aspiration lesions of the orbital frontal cortex and experienced the same sequence of tasks. Rats learned to track and discriminate between different odors reliably. These results suggest that other areas of the brain mediate odor-guided navigation following damage to the orbital frontal cortex.