A Video Demonstration of Preserved Piloting by Scent Tracking but Impaired Dead Reckoning After Fimbria-Fornix Lesions in the Rat

Summary

In a piloting scent tracking task, the ability of the rats to return to a refuge with food using visual an odor trail or using dead reckoning in infrared light, the integrated record of previous movements, demonstrates that the hippocampus is necessary for dead reckoning.

Abstract

Piloting and dead reckoning navigation strategies use very different cue constellations and computational processes (Darwin, 1873; Barlow, 1964; O’Keefe and Nadel, 1978; Mittelstaedt and Mittelstaedt, 1980; Landeau et al., 1984; Etienne, 1987; Gallistel, 1990; Maurer and Séguinot, 1995). Piloting requires the use of the relationships between relatively stable external (visual, olfactory, auditory) cues, whereas dead reckoning requires the integration of cues generated by self-movement. Animals obtain self-movement information from vestibular receptors, and possibly muscle and joint receptors, and efference copy of commands that generate movement. An animal may also use the flows of visual, auditory, and olfactory stimuli caused by its movements. Using a piloting strategy an animal can use geometrical calculations to determine directions and distances to places in its environment, whereas using an dead reckoning strategy it can integrate cues generated by its previous movements to return to a just left location. Dead reckoning is colloquially called "sense of direction" and "sense of distance."

Although there is considerable evidence that the hippocampus is involved in piloting (O’Keefe and Nadel, 1978; O’Keefe and Speakman, 1987), there is also evidence from behavioral (Whishaw et al., 1997; Whishaw and Maaswinkel, 1998; Maaswinkel and Whishaw, 1999), modeling (Samsonovich and McNaughton, 1997), and electrophysiological (O’Mare et al., 1994; Sharp et al., 1995; Taube and Burton, 1995; Blair and Sharp, 1996; McNaughton et al., 1996; Wiener, 1996; Golob and Taube, 1997) studies that the hippocampal formation is involved in dead reckoning. The relative contribution of the hippocampus to the two forms of navigation is still uncertain, however. Ordinarily, it is difficult to be certain that an animal is using a piloting versus a dead reckoning strategy because animals are very flexible in their use of strategies and cues (Etienne et al., 1996; Dudchenko et al., 1997; Martin et al., 1997; Maaswinkel and Whishaw, 1999). The objective of the present video demonstrations was to solve the problem of cue specification in order to examine the relative contribution of the hippocampus in the use of these strategies. The rats were trained in a new task in which they followed linear or polygon scented trails to obtain a large food pellet hidden on an open field. Because rats have a proclivity to carry the food back to the refuge, accuracy and the cues used to return to the home base were dependent variables (Whishaw and Tomie, 1997). To force an animal to use a a dead reckoning strategy to reach its refuge with the food, the rats were tested when blindfolded or under infrared light, a spectral wavelength in which they cannot see, and in some experiments the scent trail was additionally removed once an animal reached the food. To examine the relative contribution of the hippocampus, fimbria–fornix (FF) lesions, which disrupt information flow in the hippocampal formation (Bland, 1986), impair memory (Gaffan and Gaffan, 1991), and produce spatial deficits (Whishaw and Jarrard, 1995), were used.

Protocol

Animals

Twelve adult female Long–Evans rats (University of Lethbridge vivarium), weighing 250-300 gm, were housed in groups in wire mesh cages in a laboratory with room temperature maintained at 20–21°C and lighted on a 12 hr light/dark cycle (8 A.M. to 8 P.M.). Six rats received sham operations and six received fimbria–fornix lesions before testing.

Surgery

For sterile surgery, the rats were anesthetized with sodium pentobarbital (40 mg/kg, i.p.) and atropine methyl nitrate (5 mg/kg, i.p.). To make fimbria–fornix lesions, 1.5 mA cathodal current was passed for 40 sec through 00 stainless ....

Discussion

The experiments examined the contribution of the hippocampus to piloting versus dead reckoning navigation by exploiting a novel task in which rats were challanged to return home after an outward trip following a scented string from their refuge to a food pellet located at the end of the string. Control rats navigated efficiently using both spatial and dead reckoning strategies. The rats with fimbria–fornix lesions successfully navigated using a spatial strategy but were impaired when forced to use dead reckoning. T.......

Materials

List of materials used in this article

Name	Company	Catalog Number	Comments
Sodium pentobarbital	Reagent	Sigma-Aldrich	p3761-25g
Atropine methyl nitrate	Reagent	Sigma-Aldrich	a0382-5g
Rodent pellets	Animal food	BIO-SERV