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Rats with Fimbria-Fornix Lesions Display a Place Response in a Swimming Pool: a Dissociation Between Getting There and Knowing Where

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Rats with Fimbria-Fornix Lesions Display a Place Response in a Swimming Pool: a Dissociation Between Getting There and Knowing Where The Journal of Neuroscience, August 1995, 75(8): 5779-5788 Rats with Fimbria-Fornix Lesions Display a Place Response in a Swimming Pool: A Dissociation Between Getting There and Knowing Where Ian Q. Whishaw,’ Jean-Christophe Cassel,* and Leonard E. Jarrard3 ‘Department of Psychology, University of Lethbridge, Lethbridge, Alberta, Canada TlK 3M4, XNRS, UPR 419, Universitk Louis Pasteur, Strasbourg, France, and 3Department of Psychology, Washington and Lee University, Lexington, Virginia Some theories of hippocampal formation function postu- the platform from any location on the pool’s edge (Morris, late that it is involved in using the relationships between 1981). Rats with hippocampaldysfunction, produced by hippo- distal cues for spatial navigation. That rats with damage to campal removal (Morris et al., 1982; Sutherland et al., 1982a; the hippocampal formation are impaired in learning place Whishaw, 1987), damage to its efferents and afferents in the responses of escaping to a platform hidden just below the fimbria-fornix (Casseland Kelche, 1989; Sutherland and Rod- surface of the water of a swimming pool, supports this riguez, 1989), or cholinergic blockade (Sutherland et al., 1982b; view. Using rats with fimbria-fornix (FF) lesions, we ex- Whishaw, 1985a,b; Whishaw and Tomie, l987), are severely amined whether their impairment is related to an inability impaired. Since the samestudies show that the rats remain ex- to learn how to reach the platform as opposed to learning cellent swimmersand can quickly learn to escapeto a visible its location. In a first experiment, the FF rats were impaired platform, the results suggestthat the hippocampusis selectively in learning to swim to a hidden platform but could swim to involved in using the relational properties of ambient cues to a visible platform. In a second experiment, after being pre- guide movements. trained to swim to a visible platform, the FF rats swam to, Despite evidence that disruption of hippocampal function im- paused, and searched the vicinity of the platform’s previ- pairs spatial behavior, it is difficult to demonstratethat this is ous location when it was removed. This finding showed due to an inability to use the relations between ambient cues. that the FF rats expected to find the platform at that loca- As first demonstratedby Krechevsky (1938), problem solving tion. Additional tests confirmed that they had learned a involves at least two processes:discovering the task’s solution place response. Despite having acquired a place response, and then learning the task. Similarly, in swimming pool tasks, they still could not acquire new place responses when only animalsmust first learn to swim, discover that there is an escape, the hidden platform training procedure was used. Thus, and find that effective guidance requires distal cues (Sutherland these results in dissociating the processes of “getting and Dyck, 1984; Whishaw and Petrie, 1988). In fact, during the there” and “knowing where” suggest that the FF rats’ im- pairment may be in some process of motoric control, such first swimming trials, the rats engage in a variety of behaviors as path integration, rather than in learning the location of such as scrabbling at the edge of the pool, swimming around its the platform in relation to ambient cues. The results are edge, making sorties into the center of the pool, swimming in discussed in relation to relevant theories of hippocampal circles, etc., suggestingthat they are searchingfor an appropriate function. solution. Once a solution is found, however, new place re- [Key words: configural learning and space, fimbria-fornix sponses,even in tests in novel locations, can be acquired within and space, hippocampus and space, path integration, one trial (Whishaw, 1985c, 1989). This raises the question of place learning, rat spatial learning, spatial navigation] whether retarded place learning following hippocampaldamage residesin finding and using an appropriate solution or “getting A number of theories of hippocampal function suggest that it there,” rather than, or in addition to, loss of the ability to know has a role in using the relations between ambient cues to guide a location using ambient cues or “knowing where.” movements(Hirsh, 1974; O’Keefe and Nadel, 1978; Sutherland The presentstudy addressesthis question by demonstratingin and Rudy, 1989; Jarrard, 1993). In an exemplar task, rats placed a first experiment that rats with fimbria-fornix (FF) lesionsare in a swimming pool, in which a small escapeplatform is hidden impaired in acquiring a place response.Then in a second ex- just beneath the water’s surface, will learn to swim directly to periment, FF rats are trained with a visible cue using a gradual adaptationprocedure to determine whether first having been pro- Received Jan. 12, 1995; revised Mar. 30, 1995; accepted Apr. 6, 1995. vided with an acquisition strategy they demonstratesubsequently This research was supported by a grant from the Natural Sciences and En- that have acquired a place responseas do control rats (Whishaw gineering Research Council of Canada, by a fellowship from Ministere de la Recherche et de la Technologie to I.Q.W., and grants from the Direction des and Mittleman, 1986). Behavior is then assessedon probe trials Recherches et Etudes Techniques (93086). We thank Joanne Tomie for assis- with kinematic measuresof swim direction, distance,and veloc- tance. ity, to determine whether the rats expected to find a platform in Correspondence should be addressed to Dr. Ian Q. Whishaw at the above address. the pool and, more importantly, to determine whether they ex- Copyright 0 1995 Society for Neuroscience 0270-6474/95/l 55779- 10$05.00/O pect to find it at its previous location. In addition to this central 5780 Whishaw et al. - Place Learning in Fimbria-Fornix Rats experiment, control studies were performed to characterize fur- which the automatic systems followed the average exposed surface of ther the spatial abilities of the rats. the rat did not produce reliable results.) Histology. At the completion of the experiments, the rats were deeply anesthetized, perfused with saline and saline-formalin, and the brains Materials and Methods were removed and stored in a 30% sucrose formalin solution. The brains were cut in 40 pm sections on a cryostat and alternate sections were Methods with cresyl violet and stained for acetylcholinesterase. Animals. Thirty-six male Long-Evans rats (University of Lethbridge vivarium) were used. They were housed in pairs in plastic bowls in a laboratory with room temperature maintained at 20-21°C and lighted Procedure on a 12/12 hr light/dark cycle. For 2 weeks after surgery, the rats were Two experiments were performed. In the first experiment, the perfor- taken to the test room, removed from their cages, and handled for about mance of FF rats and control rats was assessed on a place task that 5 min. At the time the experiment began, the rats weighed 400-500 consisted of escaping to a hidden platform using conventional training gm. procedures. In the second .experiment, similar groups of rats were first Surgery. Prior to the beginning of the handling procedures, the rats trained to swim to the visible platform and were then evaluated on probe received bilateral cathodal lesions that severed the axons of the fimbria- trials to determine whether they attended to distal ambient cues. The fornix. Cathodal current was passed for 40 set through 00 stainless steel same groups were subsequently given a number of additional probe and insect pins insulated with epoxylite except at the surface of their tips. training tests to confirm that they had learned a place response. Lesions were made at two sites in ea?h hemisphere using coordinates in reference to bregma and the surface of the dura: 1.3 mm posterior, 1.5 mm lateral, and 3.6 mm ventral, and 1.5 mm posterior, 0.5 mm Experiment I: the effect of FF lesions on place learning lateral, and 3.3 mm ventral. Behavioral testing began 15 d following Eleven rats with fimbria-fornix lesions and nine control rats were used. surgery. The hidden platform was located in the NE quadrant of the pool. Each Swimming pool. The swimming pool was located in a test room in rat received two trials each day and each of the two trials began at one which many cues, including windows covered by blinds, counters, cup- of the four start locations, with starting locations changed each day. The boards, etc., were present. A 146 cm diameter and 45 cm high round trials were given sequentially with an intertrial interval of about 10 sec. white swimming pool was located in the center of the room. It was After the rats had completed 28 trials, the hidden platform was replaced filled to a depth of 25 cm with 22°C water that was made opaque with the addition of 1500 cc of powdered milk. with the visible platform for six trials. Then, the rats received two more Platforms. Depending upon the task, one of two platforms was lo- trials with the platform hidden. Trials were videorecorded, swims were cated in the pool. The visible platform was an 8.5 cm2 wooden block recorded on a map of the pool, and latency was recorded with a stop painted black that protruded from the water for 3 cm. A small shelf watch. below the surface of the water served as a step to help the rats climb onto the platform. The hidden platform was made of clear Plexiglas Experiment II: pretraining on the visible platform followed by and its 11 cm* top was located 1 cm below the surface of the water probe trials where it was not visible to a viewer on the surface of the water. The surface of the platform was serrated so that the rats could obtain pur- Training.
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