Proximal versus distal cue utilization in spatial navigation: the role of visual acuity?

Proximal versus distal cue use in the Morris water maze is a widely accepted strategy for the dissociation of various problems affecting spatial navigation in rats such as aging, head trauma, lesions, and pharmacological or hormonal agents. Of the limited number of ontogenetic rat studies conducted, the majority have approached the problem of preweanling spatial navigation through a similar proximal-distal dissociation. An implicit assumption among all of these studies has been that the animal's visual system is sufficient to permit robust spatial navigation. We challenged this assumption and have addressed the role of visual acuity in spatial navigation in the preweanling Fischer 344-N rat by training animals to locate a visible (proximal) or hidden (distal) platform using double or null extramaze cues within the testing environment. All pups demonstrated improved performance across training, but animals presented with a visible platform, regardless of extramaze cues, simultaneously reached asymptotic performance levels; animals presented with a hidden platform, dependent upon location of extramaze cues, differentially reached asymptotic performance levels. Probe trial performance, defined by quadrant time and platform crossings, revealed that distal-double-cue pups demonstrated spatial navigational ability superior to that of the remaining groups. These results suggest 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 extramaze cue location within the testing environment. The standard hidden versus visible platform dissociation may not be a satisfactory strategy for the control of potential sensory deficits.     

Development of place navigation in rats from weaning to puberty

Young hooded rats were trained to escape onto a hidden platform after swimming in a pool of opaque water. Subjects 21, 28, 35, 42, and 64 days of age on the first training day were given 28 trials on 5 consecutive days. Half of the rats were required to localize the platform in relation to external room cues only ("place only" condition) and the other half were helped by the presence of a visible cue on the platform ("cue + place" condition). A deficiency in place navigation was observed in the 21- and 28-day groups; they showed slow escape and took circuitous routes more often than older rats. This deficiency was related to a poor spatial bias toward the training position when the subjects were allowed to swim for 30 s in the absence of the platform, at the end of the 28-trial training period (probe trial). The 35-day group showed adult-like learning ability in both training conditions, but failed to show searching behavior during the probe trial after having been trained in the presence of the proximal cue. Only rats older than 40 days showed typical adult behavior such as swimming directly toward the platform from any starting position and localized searching around the absent platform's position during the probe trial, no matter what the training conditions were. These results suggest that central nervous system structures responsible for place learning in the rat are functional from around 32 days of age, but fail to trigger searching behavior following cued training before the sixth week.     

Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze

While estrogen enhances performance on some tasks of learning and memory, it has impairing or no effects on others. It has been proposed that estrogen differentially affects performance on various tasks of learning and memory by influencing the strategy used to solve a task. The goal of the present study was to determine if estrogen would influence strategy selection in the Morris water maze. Long-Evans rats were ovariectomized and implanted with Silastic capsules containing 25% estradiol diluted in cholesterol or 100% cholesterol. Rats were trained in a water maze task in which multiple strategies were available for use to locate a hidden escape platform that was moved to a new location for each set of four daily trials. During 10 days of acquisition trials, a visible floating landmark was always located in a static position relative to the hidden escape platform. Additionally, fixed extramaze cues visible to the animals surrounded the maze. Following acquisition, 2 days of probe trials were conducted in which the static landmark was removed. Estrogen replacement in ovariectomized rats resulted in impaired performance across 10 days of acquisition. Additionally, while removal of the visible landmark during the probe trials had no effect on the performance of the females receiving estrogen, it significantly disrupted performance of females receiving cholesterol treatment. These results indicate that estrogen replacement in ovariectomized rats biases an animal against using a landmark or static cue to aid in the location of a hidden escape platform in the water maze.     

Dissociation of Hippocampal and Striatal Contributions to Spatial Navigation in the Water Maze

Two experiments were conducted to compare the effects of fornix/fimbria and caudate-putamen lesions in Long–Evans hooded rats (Rattus norvegicus) trained on two water maze tasks that differed in the type of spatial localization required for optimum solution. In Experiment 1, the lesioned rats and surgical controls were trained on the standard place task in the water maze (Morris, 1981) and given two postacquisition tests (a platform removal probe and platform relocation test). In Experiment 2, rats with similar lesions and control rats were trained on a modified cue navigation task. Fornix/fimbria lesions impaired a late stage of place task acquisition but did not impair acquisition of the cue task. Caudate-putamen lesions resulted in a severe place acquisition impairment and a transient cue acquisition impairment, both of which were characterized by an initial tendency to swim near the wall of the pool. Post-hoc analyses of the direction and angles of departure from the start points suggested that rats with fornix/fimbria lesions used non-allocentric spatial strategies to solve the place task. These rats also demonstrated a significantly weakened spatial bias for the former training quadrant on the platform removal probe and reduced flexibility in navigating to a novel platform location on the platform relocation test. In contrast, rats with caudate-putamen lesions showed a significant spatial bias for the former training quadrant but failed to cross the exact location within the quadrant where the platform was formerly positioned. The results suggest that the hippocampus mediates the allocentric spatial component of the water maze place task while the dorsomedial striatum may play an important role in the acquisition of the procedural aspects of both place and cue versions of the task.     

Spatial and nonspatial escape strategies in the Barnes maze

The Barnes maze is a spatial memory task that requires subjects to learn the position of a hole that can be used to escape the brightly lit, open surface of the maze. Two experiments assessed the relative importance of spatial (extra-maze) versus proximal visible cues in solving the maze. In Experiment 1, four groups of mice were trained either with or without a discrete visible cue marking the location of the escape hole, which was either in a fixed or variable location across trials. In Experiment 2, all mice were trained with the discrete visible cue marking the target hole location. Two groups were identical to the cued-target groups from Experiment 1, with either fixed or variable escape locations. For these mice, the discrete cue either was the sole predictor of the target location or was perfectly confounded with the spatial extra-maze cues. The third group also used a cued variable target, but a curtain was drawn around the maze to prevent the use of spatial cues to guide navigation. Probe trials with all escape holes blocked were conducted to dissociate the use of spatial and discrete proximal cues. We conclude that the Barnes maze can be solved efficiently using spatial, visual cue, or serial-search strategies. However, mice showed a strong preference for using the distal room cues, even when a discrete visible cue clearly marked the escape location. Importantly, these data show that the cued-target control version of the Barnes maze as typically conducted does not dissociate spatial from nonspatial abilities.     

Visits to starts, routes, and places by rats (Rattus norvegicus) in swimming pool navigation tasks

Rats were trained to escape to visible or to hidden platforms in a swimming pool and then given probe trials, which requires that they search for a platform that had been removed or repositioned. To solve the tasks, they simultaneously used a number of behavioral strategies including position responses, cue responses, and place responses. On the probe trials, they not only displayed behaviors that were reinforced during training, including searches in the quadrant where the platform had been located and swims across the point where the platform had been, but they also displayed novel behaviors, including swims to previously used start points on the pool wall and swims that retraced previously used routes to the platform. Rats trained on the place task (hidden platform) made more swims across the platform's previous location, whereas rats trained on the cue task (visible platform) made more returns to previously used start points. When the number of start points or number of platform locations used during training was varied, swimming patterns on the probe trials also changed. Increases in the number of start points produced more returns to start points, whereas increases in the number of platform locations produced more searches for platforms. The results reveal that rats make coextensive use of all relevant strategies to solving spatial navigation tasks. Also, their search patterns on probe trials reflect previously reinforced behaviors as well as novel unconditioned search behaviors. The implications of the results for studies of the neural basis of spatial navigation and/or animal models of human memory are discussed.     

Damage to the hippocampal formation in rats selectively impairs the ability to learn cue relationships

We assessed the contribution of the hippocampal formation to performance in tasks that require rats to respond to a relationship between discriminative stimuli. The first experiment employed a nonmatching-to-sample procedure in a Y-maze. Three pairs of boxes were used which differed in brightness of the walls and in the odors that they contained. The rats were trained prior to receiving kainic acid and colchicine-induced damage to the hippocampal formation or electrolytic damage to the amygdala. After surgery all rats performed the nonmatching-to-sample task accurately if both brightness and odor cues were present in the sample and choice boxes or if the boxes contained either visual cues alone or odor cues alone. If the available cue modality was different in sample and choice boxes, then the amygdala-damaged, but not the hippocampal-damaged, rats performed accurately. In the second experiment control rats or rats with hippocampal formation damage were trained postoperatively in a conditional black/white discrimination task in a Y-maze. Only the control group successfully learned to select the white arm if the start box was illuminated and the black arm if the start box was dark. Subsequently, both groups learned a simple black/white discrimination. The same rats were tested in the hidden platform version of the Morris water task and only the control group learned to swim accurately to the goal. Both groups learned to swim accurately to a visible black platform. The results are consistent with the notion that the hippocampal formation is essential to learning that involves control exerted by a configural relationship among cues, independently of the spatial or conditional requirements of tasks.     

Vestibular stimulation disrupts acquisition of place navigation in the Morris water tank task

The significance of vestibular input for place navigation in the Morris water maze was examined in 11 hooded rats. A 5-min rotation (2 Hz) immediately preceding retrieval of an overtrained place navigation task prolonged escape latencies by about 10 s corresponding to circular swimming induced by postrotatory aftereffects, but did not otherwise interfere with target location. A 1-min rotation immediately following the acquisition trial in the working memory version of the water maze task did not deteriorate performance in the retrieval trial performed 5 min later. Two components of the acquisition trial, i.e., active search of the hidden target (up to 1 min) and latent learning during the 30-s stay on the platform, contribute almost equally to the formation of the working memory trace. A 1-min rotation immediately preceding the isolated platform learning component impaired subsequent retrieval but was ineffective when applied 3 min earlier. Latent learning was completely disrupted when the platform with the animal was rotated during the entire 30-s stay on the target platform or when the 30-s stay on the stationary platform was followed 0 or 3 min later by a 30-s rotation on the platform. The interfering effect of the latter procedure was suppressed by covering the platform with the animal by an opaque cylinder. It is concluded that vestibular cues are particularly important for the orientation of the animal in the gravitation field and for the estimation of the angles between vectors plotted from the animal toward external landmarks. Agreement between vestibular and visual signals is a prerequisite of efficient navigation.     

Hippocampus-dependent strategy choice predicts low levels of cell proliferation in the dentate gyrus

Neurogenesis continues to occur throughout life in the mammalian hippocampus. Previous research has suggested that the production of new neurons in the hippocampus during adulthood may be related to hippocampus-dependent learning and memory. However, the exact relationship between adult neurogenesis and learning and memory remains unclear. Here we investigated whether learning strategy selection is related to cell proliferation or to survival of new neurons in the hippocampus of adult male rats. We trained rats on alternating blocks of hippocampus-dependent (hidden platform) and hippocampus-independent (visible platform) versions of the Morris water task with the platform always in the same position. Following training, rats were given a probe session during which the platform was visible and in a novel location. Preferred strategy was determined by observing the initial swim path. Rats were classified as place strategy (hippocampus-dependent) users if they swam to the old platform location. Cue strategy (hippocampus-independent) users were classified as those rats that swam initially to the visible platform. Our results indicate that rats that preferentially used a place strategy had significantly lower cell proliferation than cue strategy users. However, there was no significant difference in cell survival or number of immature neurons between strategy user groups. These results suggest that low levels of cell proliferation in the dentate gyrus may be conducive or coincident with more efficient memory processing in the hippocampus.     

Those cheating rats: male and female rats use odor trails in a water-escape "working memory" task.

Three-month-old Sprague-Dawley rats were trained on a working memory win-stay (spatial delayed matching-to-sample) water-escape task with the escape platform location the same for all subjects on a given trial, a procedure that maximizes the buildup of an odor trail to the escape platform. In subsequent tests during which the location of the escape platform varied randomly between subjects, the rats, especially the females, while continuing to perform above chance level, made increased errors. Varying the platform location between subjects eliminated odor trail as a nonambiguous cue for locating the escape platform. In a second experiment females performed better than males on a reference memory odor trail discrimination task which involved following the path of like-gender "pathmaker" rats to the escape platform. The relatively poor use of odor trails by the males was associated with a high frequency of choosing a preferred choice section or returning to the choice section selected first on the immediately preceding trial (perseveration). Collectively, the two experiments demonstrate that rats can use either working memory or odor trails to locate an escape platform in a water maze, and that they, especially females, will use odor trails in a working memory task if odor trails are available. Clearly, the location of the escape platform should be varied randomly between subjects in tests of working memory.     

Rotation of Water in the Morris Water Maze Interferes with Path Integration Mechanisms of Place Navigation

The idea that place navigation in the Morris water maze is implemented by path integration between locations determined by landmark sighting was investigated in a 200-cm-diameter pool in which circular (7.2°/s) motion of water could be induced by tangentially arranged water jets. The rats were trained at 8 trials per day to navigate to an erectable platform which was raised after the rat had spent a criterion time in the target annulus (30 cm in diameter) in the midpoint of the NW quadrant. Asymptotic escape latency of 7 s was reached after 9 days in moving water (n= 8) and after 6 days in stationary water (n= 8). The group overtrained for 13 days in stable water performed well even after it was transferred to moving water. Changing the sense of rotation of water from counterclockwise to clockwise did not affect the asymptotic performance. The above findings show that overtrained rats rely on landmark sighting rather than on path integration. The influence of water movement reappeared when place navigation to a new target (SW) was examined in alternating 2-s periods of light (L) and darkness (D). On the first day, the latencies were 15.2 ± 1.2 and 22.8 ± 1.9 s in stable and moving water, respectively, but dropped to 10 s on the following day. The tracks generated in the L period were more tortuous than those generated in the D period and this difference was more pronounced in moving than in stable water. It is concluded that path integration mechanisms supporting navigation during intervals of darkness are impaired in moving water but that this impairment disappears in overtrained animals.     

Similarity in Spatial Origin of Information Facilitates Cue Competition and Interference

Two lick suppression studies were conducted with water-deprived rats to investigate the influence of spatial similarity in cue interaction. Experiment 1 assessed the influence of similarity of the spatial origin of competing cues in a blocking procedure. Greater blocking was observed in the condition in which the auditory blocking cue and the auditory blocked cue originated at the same spatial location. Recent investigations have demonstrated that manipulations that impact competition between cues trained together have similar effects on interference between cues trained apart. Therefore, Experiment 2 investigated the influence of similarity of the spatial origin in proactive interference of Pavlovian conditioning by separately pairing two auditory cues with a common outcome, originating at the same spatial location or different spatial locations. Greater proactive interference was observed in the condition in which the interfering cue and target cue originated at the same spatial location. The results are considered in light of the possibility that a similar mechanism may underlie interference between cues trained apart and cue competition between cues trained together.     

Directional learning,but no spatial mapping by rats performing a navigational task in an inverted orientation

Previous studies have identified neurons throughout the rat limbic system that fire as a function of the animal’s head direction (HD). This HD signal is particularly robust when rats locomote in the horizontal and vertical planes, but is severely attenuated when locomoting upside-down (Calton & Taube, 2005). Given the hypothesis that the HD signal represents an animal’s sense of directional heading, we evaluated whether rats could accurately navigate in an inverted (upside-down) orientation. The task required the animals to find an escape hole while locomoting inverted on a circular platform suspended from the ceiling. In Experiment 1, Long-Evans rats were trained to navigate to the escape hole by locomoting from either one or four start points. Interestingly, no animals from the 4-start point group reached criterion, even after 29 days of training. Animals in the 1-start point group reached criterion after about six training sessions. In Experiment 2, probe tests revealed that animals navigating from either 1- or 2-start points utilized distal visual landmarks for accurate orientation. However, subsequent probe tests revealed that their performance was markedly attenuated when navigating to the escape hole from a novel start point. This absence of flexibility while navigating upside-down was confirmed in Experiment 3 where we show that the rats do not learn to reach a place, but instead learn separate trajectories to the target hole(s). Based on these results we argue that inverted navigation primarily involves a simple directional strategy based on visual landmarks.     

Generalization decrement and not overshadowing by associative competition among pairs of landmarks in a navigation task

When they are trained in a Morris water maze to find a hidden platform, whose location is defined by a number of equally spaced visual landmarks round the circumference of the pool, rats are equally able to find the platform when tested with any two of the landmarks (Prados, & Trobalon, 1998; Rodrigo, Chamizo, McLaren, & Mackintosh, 1997). This suggests that none of the landmarks was completely overshadowed by any of the others. In Experiment 1 one pair of groups was trained with four equally salient visual landmarks spaced at equal intervals around the edge of the pool, while a second pair was trained with two landmarks only, either relatively close to or far from the hidden platform. After extensive training, both male and female rats showed a reciprocal overshadowing effect: on a test with two landmarks only (either close to or far from the platform), rats trained with four landmarks spent less time in the platform quadrant than those trained with only two. Experiment 2 showed that animals trained with two landmarks and then tested with four also performed worse on test than those trained and tested with two landmarks only. This suggests that generalization decrement, rather than associative competition, provides a sufficient explanation for the overshadowing observed in Experiment 1. Experiment 3 provided a within-experiment replication of the results of Experiments 1 and 2. Finally, Experiment 4 showed that rats trained with a configuration of two landmarks learn their identity.     

Manual localization of lateralized visual targets

The effects of visual field, responding limb and extrapersonal space on the ability to localize visual targets using slow positioning movements of the arm were examined. Special contact lenses were used to lateralize visual information and to make comparisons with localization under monocular control conditions. Subjects made slow positioning movements to place a cursor directly beneath target lights. They saw target lights but not the moving limb during the trial. For directional error, results indicated that subjects were more accurate localizing targets lateralized to the right hemisphere than targets lateralized to the left hemisphere, indicating right hemisphere superiority for localization of visual targets in grasping space. Localization performance was significantly better with the right hand than the left hand. the left hand demonstrated a directional bias to the right of the targets. Responding hand and visual field did not interact. Finally, contrary to subjects' awareness and verbal reports, target localization was not less accurate in lens than in monocular control conditions. This was true for both amplitude and directional error. This is consistent with other studies where visual information about limb position is not available.     

Going the distance: Extra-symbolic contributions to the symbolic control of spatial attention

Over the past 30 years, researchers have used symbolic cues such as spatial words and arrows to direct observers' attention to the location of target objects that appear at a single, fixed distance in simple visual environments; however, they have done so by using symbolic cues that provide only partial—directional—information about the spatial location of target objects. Thus, it remains unclear whether observers can only shift their attention broadly in the cued direction in response to these cues or whether they can shift their attention to the specific location of the target by combining an expectation about direction (derived from apprehension of the directional cue) with an expectation about distance (derived from some extra-symbolic cue). The results of two experiments showed that observers do shift their attention to relatively coarse spatial locations by combining expectancies about direction and distance, and that the extent to which observers do so is modulated by the presence of visible markers and the expected distance of the target. These findings are important because they provide the first evidence that extra-symbolic information about distance contributes to the symbolic control of spatial attention.     

Multiple spatial learning strategies in goldfish (Carassius auratus)

There is a considerable amount of evidence that mammals and birds can use different spatial learning strategies based on multiple learning and memory systems. Unfortunately, only a few studies have investigated spatial learning and memory mechanisms in other vertebrates. This study aimed to identify the strategies used by goldfish to solve two different spatial tasks in a series of three experiments. In experiment 1, two groups of goldfish (Carassius auratus) were trained either in a spatial constancy task (SC), in which visual cues signalled the goal indirectly, or in a directly cued task (DC) in which similar cues signalled the goal directly. Transfer tests were conducted to study the effects of discrete cue deletion on the performance in both tasks. In these transfer tests the performance of the animals trained in the DC task dropped to chance level when the cue that signalled the goal directly was removed. In contrast, the removal of any single cue did not disrupt SC performance. In experiment 2, fish trained in the SC or the DC task were trained with the goal reversed. Goldfish in the SC group needed fewer sessions to master the reversal task than DC animals. Finally, experiment 3 investigated the effects of a substantial modification of the geometrical features of the apparatus on the performance of animals trained in the SC or in the DC condition. The performance of DC goldfish was not affected, whereas the same change disrupted performance in the SC animals despite the presence of the visual cues. These results suggest that there are separate spatial learning and memory systems in fish. Whereas the DC animals used a typical guidance strategy, relying only on the cue that signalled the goal directly, SC fish relied on a strategy with the properties of an actual spatial mapping system. Thus, the comparative approach points to the generality of these learning strategies among vertebrates. Received: 10 October 1998 / Accepted after revision: 16 April 1999     

The relative influence of place and direction in the Morris water task

Previous work from our laboratory has demonstrated that rats display a preference for directional responding over true place navigation in the Morris water task. The present study evaluated the range of situations in which this preference is observed and attempted to identify methods that favor navigation to the precise location of the escape platform in the room. A preference for directional responding over place navigation was observed in a wide range of procedures that included providing extensive training (Experiment 1), providing only platform placement experience in the absence of active swim training (Experiment 2), training navigation to multiple platform locations in a moving platform variant of the task (Experiment 3), and explicitly training navigation to a precise location in the room, versus navigation in a particular direction, regardless of the pool's position in the room (Experiments 4-5). A modest preference for navigation to the precise spatial location of the platform was observed when the pool wall was virtually eliminated as a source of control by filling it to the top with water (Experiment 6).     

Transient spatial attention and the perceived duration of brief visual events

This study was designed to explore the effects of transient attention—the stimulus-driven component of spatial attention—on the perceived duration of a brief visual event. Observers had to compare the duration of two disks presented successively within a single trial. The disks’ location and duration varied independently. One of these disks, the “attended disk”, was preceded by an attentional cue indicating the disk's location, attracting transient attention in advanced to the disk location. This attentional cue was either a typical onset cue (Experiments 1, 2, and 4) or a singleton cue (Experiment 3) that minimized the differences between the cues. The other disk, the “neutral disk”, was cued with a neutral cue that did not convey information regarding the disk location. We found that the attraction of transient attention to the location of the attended disk prolonged its perceived duration, but only when compared to brief nonattend stimuli.     

Effects of Unilateral Entorhinal Cortex Lesion on Retention of Water Maze Performance

In a previous study, adult male Sprague-Dawley rats with unilateral, electrolytic entorhinal cortex lesions showed significant deficits in acquisition of a water maze task that measured working memory. The 10 days of testing used two trials per day with an intertrial interval of 1 h, and the rats with entorhinal damage were impaired in total distance to the platform in both trials. In the present retention study, rats who learned the same task prior to injury and were then retested for 5 days after lesion showed only a first day deficit in total distance to platform in the second trial. Analysis of swim patterns indicated that rats with unilateral entorhinal lesions used an altered strategy in retention testing to find the platform in the second trial of each day and incorporated the use of headings appropriate for Trial 1 only. This altered or compensatory strategy was not the optimum choice for problem solution. Although the rats then were able to switch headings and find the platform without significant impairment in total distance to platform on days 2–5 of testing, the use of an initial incorrect strategy indicated subtle residual deficits in cue integration and use of working memory.