Comparison of developmental trajectories for place and cued navigation in the Morris water task

Previous studies investigating the development of place and cued learning using the Morris water task are in disagreement regarding the day in development that each type of learning emerges. Here, place and cued navigation in the water task were examined in differently aged groups of young male and female rats (P17, P18, P19, P20, and P24) during a single day of training. When only distal cues were present, P20 and P24 but not younger rats learned the location of the hidden platform. In contrast, when a proximal cue marked the platform location, rats as young as P17 showed evidence of cue-controlled navigation, although only P18 and older rats exhibited cued learning. In line with most previous studies, these results indicate that cued learning emerges earlier in development than place learning and support a dissociation of developmental trajectories for the neural systems underlying the two types of navigation.     

Use of salient and non-salient visuospatial cues by rats in the Morris Water Maze

In the Morris Water Maze (MWM), an animal learns the location of a hidden platform relative to distal visual cues in a process known as spatial learning. The visual cues used in MWM experiments are invariably salient in nature, and non-salient cues, such as subtle environmental variations, have not traditionally been considered to play a significant role. However, the role of non-salient cues in spatial navigation has not been adequately investigated experimentally. The objective of this experiment was therefore to determine the relative contribution of salient and non-salient visual cues to spatial navigation in the MWM. Animals were presented with an environment containing both types of visual cues, and were tested in three successive phases of water maze testing, each with a new platform location. Probe tests were used to assess spatial accuracy, and several cue variation trials were run in which both salient and non-salient visual cues were manipulated. It was observed that removal of the salient visual cues did not cause a significant deterioration in performance unless accompanied by disruption of the non-salient visual cues, and that spatial navigation was unimpaired when only the salient visual cues were removed from view. This suggests that during place learning in Long-Evans rats, non-salient visual cues may play a dominant role, at least when salient cue presentation is limited to four cues.     

Ontogeny of spatial navigation behaviors in the rat: dissociation of "proximal"- and "distal"-cue-based behaviors

Rats can use both "proximal" and "distal" cues to locate goal objects in their environments (Morris, 1981). In the proximal-cue situation, local stimuli that spatially co-occur with the goal are available to guide behavior. In the distal-cue situation, there are no cues that co-occur with the goal object; thus to directly locate the goal, the rat must learn about the spatial location of the goal relative to distal cues. Using the Morris water maze, we found that these two navigation behaviors are dissociated during ontogeny. Rats only 17-days-old are capable of using proximal cues to locate a safe platform. It was not until the rats were 20-days-old, however, that they began to display minimal evidence of distal-cue utilization. Control experiments indicated that the 17-day-old subjects' failure on the distal problem was likely due to their inadequate spatial learning skills. These results were interpreted within a Jacksonian perspective of brain-behavior relations.     

Preweanling rats solve the Morris water task via directional navigation

Adult rats show a preference for directional navigation over place navigation in the Morris water task. Here, the authors investigated whether preweanling rats with a newly developed ability to perform the water task also solve the task via directional navigation. After 24-day-old rats were trained to find a hidden platform in a fixed spatial location, a no-platform probe trial was conducted with the pool either in the same position as that used during training (no shift group) or shifted to a new position in the room (shift group). The authors found that rats in the shift group did not search for the platform at its absolute spatial location but rather navigated in the same direction that the platform was located during training and searched at the correct distance from the pool wall, resulting in a search at a location that was never trained. This pattern of results suggests that young rats learn to solve the water task by navigating in a particular direction rather than navigating to a precise place--a finding that may have implications for understanding hippocampal development.     

Proximal versus distal cue utilization in preweanling spatial localization: the influence of cue number and location

The present study was designed to examine the role of cue location and number in spatial navigation of the preweanling Fischer-344N rat in the Morris water maze using a protocol consistent with the pups' response repertoire. The proximal (visible platform) versus distal (hidden platform) cue strategy was used, and spatial cues within the extramaze environment were configured such that the arrangement presented either a double cue or null cull condition relative to the platform location. All pups' performance improved with training; however, probe trial performance, defined by quadrant time and platform crossings, revealed distal-double cue pups demonstrated spatial navigational ability superior to the remaining groups. This experimental dissociation suggests that a pup's ability to spatially navigate a hidden platform is dependent on not only its response repertoire and task parameters but also its visual acuity, as determined by the number of extramaze cues and the location of these cues within the testing environment. The hidden versus visible platform dissociation may not be a satisfactory strategy for the control of potential sensorimotor deficits.     

Use of proximal and distal cues in place navigation by mice changes during ontogeny

The ontogeny of the ability of C57BL/6 mice to use different cues for spatial learning was examined in several Morris water maze tasks. In the first two studies, three learning procedures were used, in which only distal cues (place learning), only proximal cues (cue learning), or both proximal and distal cues (cue + place learning) were pertinent to localize the platform. The results indicated that whatever the procedure, 22-day-old mice showed the same capabilities as adults. Moreover, in the cue + place-learning procedure, although the distal cues were not necessary to solve the task, both young and adult mice demonstrated the integration of distal information by exhibiting a strong spatial bias during a probe test. However, in the third experiment, it was shown that nonpertinent proximal cues perturbed 22-day-old mice in a place-learning procedure. Taken together, these results suggest that while even the youngest mice show striking spatial navigation abilities, young mice give greater importance to proximal cues for orientation whereas adults preferentially use distal information. © 1996 John Wiley & Sons, Inc.     

Medial septal lesions disrupt spatial mapping ability in rats

Rats with lesions of the medial septum were more likely to begin swimming in the wrong direction, swim farther, and, therefore, require more time to find a platform hidden in a Morris water tank than were control rats. Although the performance of the rats with medial septal lesions did improve over trials, their asymptotic performance also failed to equal that of the controls. Movement of the platform to a new position in the tank disrupted the performance of both groups, and, again, the rats with medial septal lesions were slower to locate the moved platform. However, this deficit was completely eliminated when a visual cue indicating the location of the moved platform was introduced. We suggest that these data indicate that damage to the septo-hippocampal cholinergic projection system produces a deficit in the formation or utilization of a spatial map (reference memory) that represents the location of a place with respect to the surrounding distal cues.     

Cholinergic receptor blockade produces impairments in a sensorimotor subsystem for place navigation in the rat: evidence from sensory, motor, and acquisition tests in a swimming pool

Studies have shown that central cholinergic receptor blockade biases the behavior of rats so that they make less use of the sensorimotor behaviors that are normally used to orient to the relational properties of distal cues and that they simultaneously become more reliant on proximal cues. In Experiment 1, control rats and rats treated with atropine sulfate or atropine methyl nitrate (50 mg/kg) were trained to escape to a visible platform from different starting points in a swimming pool. All groups learned the task by concomitantly developing position responses, by orienting according to room cues, and by orienting to the platform, but probe trials showed that the atropine-sulfate group made more use of the platform as a local cue and made less use of distal cues than did the other groups. The atropine-sulfate group also made fewer searches during acquisition, made fewer searches when the platform was removed on probe trials, and were less responsive to novel cues placed above and around the pool. Swim speed, as estimated by the distance swum on probe trials, was also greater in atropine-sulfate-treated rats. The postulate that rats treated with atropine sulfate preferentially guide swimming by using position responses and local cues was tested in Experiment 2 by comparing their performance with that of control rats in a place task in which a target platform was hidden (no local cues present) and in a similar place task in which the target platform was visible, as was a second incorrect platform that sank when climbed upon (two competing local cues present). Although both tasks were acquired by the control and drugged rats, the two-platform task, as predicted, was comparatively more difficult for the atropine-treated rats. These results suggest that one effect of central cholinergic blockade is to impair the use of a sensorimotor subsystem used for place navigation.     

Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool

Normal rats and rats drugged with atropine sulfate, a cholinergic muscarinic blocker, were evaluated in the Morris water task for their use of spatial navigation strategies. Atropine-treated rats were impaired on a place response of swimming to a platform hidden in a pool filled with opaque water. With extended training, they did learn the place response, though not with control precision, as shown by better than chance heading angles upon swim initiation, searches in the old location for a platform that had been moved, and by correct swims from novel starting locations. Acquisition could not be accounted for by habituation to the drug. In contrast with the acquisition deficit, pretrained rats were relatively unimpaired by the drug. In separate experiments, the strategies used by the drugged animals were examined. Atropine-treated rats were not impaired in acquisition or retention of a cue task, swimming to a visible platform, or a position response task, turning left to locate a platform, but both control and atropine-treated rats were unable to reverse position responses. Possibly, atropine-treated rats can use cue and position response strategies in part or in combination to acquire a place response. Atropine-treated rats were unable to acquire a place learning set, which involved swimming to a new location each day, a response that is eventually performed by normal rats in approximately one trial. They also were unable to perform a learning-set response, which they had acquired when undrugged. Insofar as the impairments following atropine are characteristic of a deficit in the use of a locale strategy, that is, making rapid use of relational properties of distal cues, whereas their successes are characteristic of the use of taxon strategies, that is, cue or position responses, the results suggest that locale systems of navigation are more importantly dependent on cholinergic brain mechanisms than taxon strategies. The resistance of preacquired place responses to atropine may suggest that normally rats acquire place responses by using a locale strategy but effect rehearsed responses by using taxon strategies. Finally, characteristic differences in acquisition, retention, and reversal of atropine-treated and control rats using different navigational strategies suggest new possibilities for interpreting various performance features displayed by animals after other types of treatment.     

Ontogeny of spatial navigation in rats: a role for response requirements?

Three experiments investigated the role of response requirements in the Morris water maze for pre- and postweanling rats. Fischer-344N pups were required to locate a hidden platform using extramaze cues in a tank modified for the pups' immature response repertoire. Weanlings (20-22 days) displayed spatial learning in a pool 1/2 the size of the adults' (Experiment 1); by 26-28 days of age, probe performance was comparable to adults' on quadrant preference and platform-crossing measures. Preweanlings (17 days), in a pool 1/3 the original size, significantly reduced escape latencies and displayed quadrant preference and platform-crossing scores indicative of spatial navigation. These results suggest that despite its protracted postnatal development, the preweanling hippocampus allows neural integration of visual-spatial information; however, the capacity to demonstrate such learning is dependent on task parameters and the pup's response repertoire.     

Long-term retention of spatial navigation by preweanling rats

The present study was designed to examine retention of spatial information in the immature, Fischer-344N rat using a savings paradigm. Following training to locate a hidden platform using extramaze cues, preweanling animals (17 days of age) were immediately probed by testing in the tank with the platform removed. One week later, pups (26 days of age) were given an additional four training trials immediately followed by a second probe test to examine the animals' memory for the location of the platform. Animals that received initial training at 17 days of age demonstrated significant savings of information when tested after the retention interval. These data replicate our recent report of spatial navigation capabilities in the preweanling rat, and extend those findings by demonstrating that preweanling spatial navigation performance permits more rapid and accurate navigation following a 7-day retention interval after a "reinstatement" insufficient to produce accurate navigation in maturation controls.     

Auditory cued spatial learning in mice

Spatial learning based on auditory cues was examined by C57BL mice in dry versions of the Morris water maze task in a dark room. One speaker was placed outside of the maze in the first task and two speakers emitting different sounds were placed outside the maze in the second task. The mice could learn the position of food in both tasks. Performance was disrupted when the auditory cue was removed, but they performed well when the position of the sound and food were shifted to a fixed spatial relationship. Results demonstrate the ability of auditory cued spatial navigation in mice.     

Deficits of Morris water maze learning in rats with striatal kainic acid lesions

This study investigated effects of intrastriatal kainic acid administration, which induces selective neuronal cell death in the striatum sparing passing nerve fibers and terminals, on the acquisition of spatial learning in Morris water maze. Rats treated with bilateral kainic acid (0.5-1.0 microgram) into the striatum were trained to escape to a hidden platform under the water. Compared with control rats, kainic acid (1.0 microgram)-lesioned rats showed significantly longer escape latency in the place navigation, and in the following probe test lower rate of swimming within the quadrant where the platform had been placed. In addition, kainic acid (1.0 microgram)-lesioned rats showed longer latency in the cue navigation in which rats were trained to escape to a visible platform above the water. These deficits were caused by their tendency to swim along the wall of pool before approaching the platform and not by their swim difficulty. Results suggest that striatal neurons or neural circuits containing these neurons play an important role in the acquisition of spatial learning task, and the nature of this performance impairment was discussed in terms of both learning and attention deficits.     

Similarities in the development of place and cue navigation by rats in a swimming pool

The development of place and cue spatial navigation was evaluated in 18-, 19-, and 20-day-old males in the Morris water task (MWT). Past work has suggested that place and cue learning develop at different rates, suggesting that the two aspects of spatial navigation have different neural substrates. In the present study, a new training methodology was used in which animals received spaced training trials, drying and warming in between trials to maintain body temperature, and two probe trial-dependent measures to evaluate spatial memory performance. All ages of rats had lower latencies on the cue task than on the place task. Nevertheless, 18-day-old rats did not learn either task as measured by acquisition latencies and probe trial-dependent measures. The 19- and 20-day-old rats learned both the place and cue tasks as measured by acquisition latency and direct swims to the correct platform location on the probe trial, and both 19- and 20-day-old rats demonstrated a strong spatial bias to the former platform location on the place probe trial but not on the cue probe trial. The finding that developmental onset of place and cue spatial navigation is rapid and complete by day 19 is discussed in relation to contemporary theories of spatial navigation.     

An evaluation of spatial information processing in aged rats

The spatial learning abilities of young, middle-age, and senescent rats were investigated in two experiments using several versions of the Morris water maze task. In Experiment 1, Long-Evans hooded rats were trained to find a submerged escape platform hidden within the water maze. During this phase of testing, aged rats exhibited acquisition deficits compared with either young or middle-age subjects. With continued training, however, all age groups eventually achieved comparable asymptotic levels of performance. Subsequent testing in Experiment 1 revealed that following original training, aged rats were not impaired in learning a novel escape location or in their ability to locate a visible, cued escape platform. In an attempt to identify the basis of the age-related impairments observed in Experiment 1, naive young and aged rats in Experiment 2 were initially tested for their ability to locate a cued escape platform in the water maze. During this phase of testing, the escape latencies of both young and aged rats rapidly decreased to equivalent asymptotic levels. Subsequent analyses revealed that following cue training, young subjects exhibit a significant spatial bias for the region of the testing apparatus where the platform was positioned during training. In contrast, aged rats showed no spatial bias. Training was continued in Experiment 2 using a novel submerged platform location for each subject. During these place training trials, the escape latencies of senescent rats were longer than those of young subjects. These impairments were also accompanied by a lack of spatial bias among aged rats relative to young control subjects.(ABSTRACT TRUNCATED AT 250 WORDS)     

Spatial learning and memory following fimbria-fornix transection and grafting of fetal septal neurons to the hippocampus

Summary The ability of intrahippocampal grafts of fetal septal-diagonal band tissue, rich in developing cholinergic neurons, to ameliorate cognitive impairments induced by bilateral fimbria-fornix transections in rats was examined in three experiments using the Morris water-maze to test different aspects of spatial memory. Experiment 1. Rats with fimbria-fornix lesions received either septal cell suspension grafts or solid septal grafts; normal rats and rats with lesions alone were used as controls. Sixteen weeks after surgery, the rats' spatial learning and memory were tested in the water-maze using a place test, designed to investigate place navigation performance, in which rats learned to escape from the water by swimming to a platform hidden beneath the water's surface. After 5 days of training, the rats were given a spatial probe test in which the platform was removed from the tank to test spatial reference memory. Experiment 2. The same rats used in Exp. 1 were tested in a delayed-match-to-sample, working memory version of the water-maze task. The platform was located in one of two possible locations during each trial, which was composed of 2 swims. If the rat remembered the location of the platform on the 2nd swim of a trial, it should find the platform more quickly on that swim, and thereby demonstrate working memory. Experiment 3. Prior to receiving fimbria-fornix lesions, normal rats were trained in a modification of the water-maze task using alternating cue navigation and place navigation trials (i.e., with visible or non-visible escape platforms). The retention and reacquisition of the place task and the spatial probe test were examined in repeated tests up to 6 months after the lesion and intrahippocampal grafting of septal cell suspensions. The effects of central muscarinic cholinergic receptor blockade with atropine were also tested. Normal rats performed well in both the place and spatial probe tests. In contrast, rats with fimbria-fornix lesions only were unable to acquire or retain spatial information in any test. Instead, these rats adopted a random, nonspatial search strategy, whereby their latencies to find the platform decreased in the place navigation tasks. Sixty to 80% of the rats with septal suspension or solid grafts had recovered place navigation, i.e., the ability to locate the platform site in the tank, in Exp. 1 and 3, and they showed a significantly improved performance in the working memory test in Exp. 2. Atropine abolished the recovered place navigation in the grafted rats, whereas normal rats were impaired to a lesser extent. In contrast, atropine had no effect on the non-spatial strategy adopted by rats with fimbria-fornix lesions only. The results show that: (1) fimbria-fornix lesions disrupt spatial learning and memory in both naive and pretrained rats; (2) with extended training the fimbria-fornix lesioned rats develop an efficient non-spatial strategy, which enables them to reduce their escape latency to levels close to those of intact controls; (3) intrahippocampal septal grafts can restore the ability of the lesioned rats to use spatial cues in the localization of the platform site; and (4) the behavioural recovery produced by grafts is dependent upon an atropine sensitive mechanism.     

Rats with hippocampal lesions learn about allocentric place cues in a non-navigational task

Hippocampal-lesioned rats (HPC) and sham controls (SH) learned constant-negative visual discriminations among scenes in a Y-maze. Any arm could be start arm for a trial. Two choice scenes ("constant" and "variable") were shown in the other arms. In Experiment 1, each problem had 2 constants. One or the other constant appeared on every trial, and the variable changed every trial; choosing the variable was rewarded. There were 4 problem types. Each constant might be always in a given direction from the start arm (added egocentric [Ego] cue), always in a given maze arm (added allocentric [Allo] cue), both, or neither. SH rats' visual learning was enhanced by Ego and by Allo cues. HPC rats' visual learning was enhanced by Ego cues, and by Allo cues, but only if there was no Ego cue. Experiment 2 confirmed that Allo cues helped HPC rats as much as SH, in the absence of Ego cues. Rats with HPC lesions can learn about allocentric place cues when navigation and idiothetic cue control are not required.     

The effect of early experience on water maze spatial learning and memory in rats

In the first of two experiments on spatial competence, groups of light-reared (LR) and dark-reared (DR) rats were compared using a "latent learning" variation of the Morris Water Maze task. On their initial test, the LR rats benefited more than DR rats did from viewing the room/pool from a platform in the correct location. Further, visually experienced rats remember the location of the platform more than DR rats when retested one month later. In a second experiment, in which a proximal cue as well as location was varied from trial to trial. LR rats again proved to be more competent than their DR counterparts. This second task also revealed significant benefits related to stimulation history in the case of a third group of animals raised in enriched or complex environment (CR) conditions. The results are discussed in terms of the nature of the impact of early experience on the ability to acquire and remember spatial concepts.     

Intracranial self-stimulation facilitates a spatial learning and memory task in the Morris water maze

Learning and memory improvement by post-training intracranial self-stimulation has been observed mostly in implicit tasks, such as active avoidance, which are acquired with multiple trials and originate rigid behavioral responses, in rats. Here we wanted to know whether post-training self-stimulation is also able to facilitate a spatial task which requires a flexible behavioral response in the Morris water maze. Three experiments were run with Wistar rats. In each of them subjects were given at least five acquisition sessions, one daily, consisting of 2-min trials. Starting from a random variable position, rats had to swim in a pool until they located a hidden platform with a cue located on its opposite site. Each daily session was followed by an immediate treatment of intracranial self-stimulation. Control subjects did not receive the self-stimulation treatment but were instead placed in the self-stimulation box for 45 min after each training session. In the three successive experiments, independent groups of rats were given five, three and one trial per session, respectively. Temporal latencies and trajectories to locate the platform were measured for each subject. Three days after the last acquisition session, the animals were placed again in the pool for 60 s but without the platform and the time spent in each quadrant and the swim trajectories were registered for each subject. A strong and consistent improvement of performance was observed in the self-stimulated rats when they were given only one trial per session, i.e. when learning was more difficult. These findings agree with our previous data showing the capacity of post-training self-stimulation to improve memory especially in rats with little training or low conditioning levels, and clearly prove that post-training self-stimulation can also improve spatial learning and memory.     

The effects of hippocampal lesions on response, direction, and place learning in rats

Rats with hippocampal or sham lesions were trained to find food on a T maze located at 2 positions. Response rats were required to make a right or left turn. Direction rats were required to go in a consistent direction (east or west). Place rats were required to go to a consistent location, relative to room cues. One place group had distinguishable start points at the 2 maze positions, whereas another place group had start points facing the same side of the room. Controls took longer to solve a place problem than the response and direction problems when the start points were not distinguishable. Rats with hippocampal lesions were not different than controls on the response problem but were impaired on the direction and place problems.