The role of the hippocampus in passive and active spatial learning.

Rats with lesions of the hippocampus or sham lesions were required in four experiments to escape from a square swimming pool by finding a submerged platform. Experiments 1 and 2 commenced with passive training in which rats were repeatedly placed on the platform in one corner-the correct corner-of a pool with distinctive walls. A test trial then revealed a strong preference for the correct corner in the sham but not the hippocampal group. Subsequent active training of being required to swim to the platform resulted in both groups acquiring a preference for the correct corner in the two experiments. In Experiments 3 and 4, rats were required to solve a discrimination between different panels pasted to the walls of the pool, by swimming to the middle of a correct panel. Hippocampal lesions prevented a discrimination being formed between panels of different lengths (Experiment 3), but not between panels showing lines of different orientations (Experiment 4); rats with sham lesions mastered both problems. It is suggested that an intact hippocampus is necessary for the formation of stimulus-goal associations that permit successful passive spatial leaning. It is further suggested that an intact hippocampus is not necessary for the formation of stimulus-response associations, except when they involve information about length or distance.

Association rules for rat spatial learning: the importance of the hippocampus for binding item identity with item location.

Three cohorts of rats with extensive hippocampal lesions received multiple tests to examine the relationships between particular forms of associative learning and an influential account of hippocampal function (the cognitive map hypothesis). Hippocampal lesions spared both the ability to discriminate two different digging media and to discriminate two different room locations in a go/no-go task when each location was approached from a single direction. Hippocampal lesions had, however, differential effects on a more complex task (biconditional discrimination) where the correct response was signaled by the presence or absence of specific cues. For all biconditional tasks, digging in one medium (A) was rewarded in the presence of cue C, while digging in medium B was rewarded in the presences of cue D. Such biconditional tasks are "configural" as no individual cue or element predicts the solution (AC+, AD-, BD+, and BC-). When proximal context cues signaled the correct digging choice, biconditional learning was seemingly unaffected by hippocampal lesions. Severe deficits occurred, however, when the correct digging choice was signaled by distal room cues. Also, impaired was the ability to discriminate two locations when each location was approached from two directions. A task demand that predicted those tasks impaired by hippocampal damage was the need to combine specific cues with their relative spatial positions ("structural learning"). This ability makes it possible to distinguish the same cues set in different spatial arrays. Thus, the hippocampus appears necessary for configural discriminations involving structure, discriminations that potentially underlie the creation of cognitive maps.

Negative patterning in the spatial domain.

In three experiments, animals were required to learn about the presence or absence of a hidden platform in a swimming pool. This was determined with reference to different patterned landmarks. In Experiment 1, the presence of a spotted or a striped cue indicated the position of the platform, while the combination of patterns, a half-spotted and half-striped cue, predicted the absence of the goal (i.e., negative patterning). In Experiment 2 the task was redesigned to better represent a locale navigation task. Rats received the same discrimination task, but it took place in an equilateral triangle with landmarks positioned on the walls of the arena. The hidden platform (if present) was located in one corner of the triangle. Experiment 3 used a more complex negative patterning discrimination in the triangular swimming pool to help dissociate between the unique cue and configural associative learning theories. Experiment 1 and 2 provides the first instance of negative patterning in a spatial task, while Experiment 3 provides initial evidence that some rats may represent compound stimuli in a way explained by the unique cue theory of associative learning. This begins to elucidate the underlying of associate principles that guide learning in the spatial domain.

The effect of schizotypy on spatial learning in an environment with a distinctive shape.

In two experiments, participants completed the Oxford-Liverpool Inventory of Feelings and Experiences measuring schizotypal traits across four dimensions (unusual experiences, cognitive disorganization, introvertive anhedonia, and impulsive non-conformity). They then took part in a virtual navigation task where they were required to learn about the position of a hidden goal with reference to geometric cues of a rectangular arena or rely on colored wall panels to find the hidden goal in a square-shaped arena. Unusual experience and cognitive disorganization were significant predictors of the use of geometric cues, but no significant predictors were found for the use of wall panels. Implications to hippocampal function and the clinical domain are considered.

Potentiation and overshadowing between landmarks and environmental geometric cues.

Rats were required in three experiments to find one of two submerged platforms that were situated in the same pair of diagonally opposite corners of a rectangular grey swimming pool. The experimental groups were trained with landmarks, comprising A4 cards attached to the walls, located in the corners containing the platforms. For the control groups, the landmarks were situated in the corners containing the platforms for half of the trials, and in the other corners for the remaining trials. Learning about the positions of the platforms with reference to the shape of the pool was overshadowed in the experimental groups when the landmarks were white, and enhanced when the landmarks were black. A fourth experiment assessed whether geometric cues influenced the control acquired by the landmarks. As in the previous experiments, the presence of the geometric cues overshadowed learning about the landmarks when they were white, but enhanced learning when the landmarks were black.

Between-cue associations influence searching for a hidden goal in an environment with a distinctive shape.

In Experiment 1 rats had to escape from a kite-shaped pool by swimming to a submerged escape platform in a right-angled corner. The two walls creating this corner were white and the two walls creating the opposite, incorrect, right-angled corner were black. The rats were then trained in a square pool with two white walls forming one corner and two black walls forming the opposite corner. The platform was in the white corner for a consistent group and the black corner for an inconsistent group. A test in an entirely white kite revealed a stronger preference for the correct than the incorrect corner in the consistent but not the inconsistent group. This outcome is attributed to the formation of associations between geometric cues, provided by the shape of the pool, and the color of the walls. The results were replicated in a second experiment in which the walls of the test pool were the same color as the incorrect corner during initial training.

Absence of overshadowing between a landmark and geometric cues in a distinctively shaped environment: a test of Miller and Shettleworth (2007).

Rats in the first 2 experiments, which were designed to test predictions from a model of spatial learning by N. Y. Miller and S. J. Shettleworth (2007), had to escape from a triangular pool by swimming to a submerged platform in a geometrically unique corner. A spherical landmark was suspended above the platform for an overshadowing group. A control group was trained with the same arrangement and with a second, identical landmark suspended in another corner. The platform could thus be found by reference to the landmark or the geometric cues in the overshadowing group, whereas the control group had to rely on geometric cues. There was no indication of overshadowing between the geometric cues and the landmark in the overshadowing group. The final 2 experiments revealed that the absence of overshadowing was not a consequence of the landmark being an ineffective cue for overshadowing. The results indicate either that the landmark and geometric cues were not in competition for the control they acquired over behavior or that an additional process compensated for any such competition that might have occurred in the overshadowing group. This additional process could involve between-cues associations or the provision of a stable spatial framework.

Where am I? Distal cues use requires sensitivity to start location change in the rat.

Place learning is impaired when a single plus maze is moved between adjacent locations 33-120 cm apart. This maze translation creates distinct start locations but maintains a single goal location with respect to distal cues. Hippocampal cell recording data suggest the majority of place fields are tied to apparatus boundaries, not to distal cues, when an apparatus is moved these distances to the left or right. Thus, rats may fail to appreciate the existence of multiple start locations with respect to distal cues when the maze is moved in this way and their start location on the surface is constant. Performance on the single plus maze problem was improved when texture cues were correlated with different start locations. Place learning was supported when multiple start locations were provided on a single large surface (double plus maze), even though rats did not explore the entire surface. Place learning was also supported when random extensions were added to a double plus maze such that start locations, relative to surface boundaries, were not informative as to goal location. This outcome suggests sensitivity to multiple start locations is required for distal cue use in translational place problems.

The influence of excitatory and inhibitory landmarks on choice in environments with a distinctive shape.

In two experiments rats were trained to find one of two submerged platforms that were located in diagonally opposite corners-the correct corners-of a rectangular pool. Additional training was given to endow two different landmarks with excitatory and inhibitory properties, by using them to indicate where a platform was or was not located in either a rectangular (Experiment 1) or a square pool (Experiment 2). Subsequent test trials, with the platforms removed from the pool, revealed that placing the excitatory landmark in each of the four corners of the rectangle resulted in more time being spent in the correct corners than when the four corners contained inhibitory landmarks. This result is contrary to predictions derived from a choice rule for spatial behavior proposed by Miller and Shettleworth (2007).

The neural basis of nonvisual object recognition memory in the rat.

Research into the neural basis of recognition memory has traditionally focused on the remembrance of visual stimuli. The present study examined the neural basis of object recognition memory in the dark, with a view to determining the extent to which it shares common pathways with visual-based object recognition. Experiment 1 assessed the expression of the immediate-early gene c-fos in rats that discriminated novel from familiar objects in the dark (Group Novel). Comparisons made with a control group that explored only familiar objects (Group Familiar) showed that Group Novel had higher c-fos activity in the rostral perirhinal cortex and the lateral entorhinal cortex. Outside the temporal region, Group Novel showed relatively increased c-fos activity in the anterior medial thalamic nucleus and the anterior cingulate cortex. Both the hippocampal CA fields and the granular retrosplenial cortex showed borderline increases in c-fos activity with object novelty. The hippocampal findings prompted Experiment 2. Here, rats with hippocampal lesions were tested in the dark for object recognition memory at different retention delays. Across two replications, no evidence was found that hippocampal lesions impair nonvisual object recognition. The results indicate that in the dark, as in the light, interrelated parahippocampal sites are activated when rats explore novel stimuli. These findings reveal a network of linked c-fos activations that share superficial features with those associated with visual recognition but differ in the fine details; for example, in the locus of the perirhinal cortex activation. While there may also be a relative increase in c-fos activation in the extended-hippocampal system to object recognition in the dark, there was no evidence that this recognition memory problem required an intact hippocampus.

Latent spatial learning in an environment with a distinctive shape.

Four experiments were conducted with rats in order to determine whether being placed on a platform in one corner of a rectangular swimming pool results in latent spatial learning. Rats in Experiments 1-3 received four trials a day of being placed on the platform. During a subsequent test trial, in which they were released into the pool without the platform, the rats exhibited a preference for swimming in the correct corners of the pool (those with the same geometric properties as the corner containing the platform during training), than the two remaining, incorrect corners. This effect was seen when the interval between the final placement trial and the test trial was as much as 24 hr (Experiment 2) and after varying numbers of sessions of placement training (Experiment 3). Experiment 4 revealed that when the test took place in a kite-shaped arena, after placement training in a rectangle, a stronger preference was shown for the corner that was geometrically equivalent to the correct rather than the incorrect corners in the rectangle. The placement treatment is said to result in latent spatial learning based on the development of S-S associations.

Changes in attention to relevant and irrelevant stimuli during spatial learning.

Rats were trained in 2 experiments to find a submerged platform that was situated in 1 of 2 of the 4 corners of a rectangular pool with a curved long wall. Different landmarks occupied 2 of the corners on every trial, and the platform was always situated near a landmark. For the place group in each experiment, the location of the platform was indicated by the shape of the pool and stimuli outside the pool (place cues), but not the landmarks within the pool. For the landmark groups, the landmarks, not the place cues, indicated where the platform could be found. During Stage 2, 2 of the place cues were relevant, and 2 of the landmarks were irrelevant, for a new discrimination. The place cues better controlled searching for the platform in the place group than in the landmark group when the place cues had initially been relevant by signaling the presence (Experiment 1) or the absence (Experiment 2) of the platform. The results show that animals pay more attention to relevant than irrelevant cues.

Conditioned inhibition and superconditioning in an environment with a distinctive shape.

In Experiments 1 and 2a rats received an A+/AX- discrimination in a rectangular pool with two submerged platforms in diagonally opposite corners-the correct corners-for A+ trials. For AX- trials, rats were placed in the pool without the platforms but with identical landmarks, X, in the correct corners. Landmark X subsequently passed both a summation and retardation test for inhibition in Experiment 1. Upon completion of the discrimination in Experiment 2a, the platforms were placed near identical landmarks in the correct corners of the rectangle. The landmarks were those used for discrimination training for a superconditioning group (AX+ trials), but for a control group they were novel (AY+ trials). During a final test in the pool without the landmarks and the platforms, the superconditioning group spent more time than the control group searching in the correct corners. This finding, which was replicated in a kite-shaped pool in Experiment 2b, demonstrates successful superconditioning by landmark X of the cues created by the shapes of the pools. The results pose a problem for the theory of Miller and Shettleworth (2007).

Spatial learning based on boundaries in rats is hippocampus-dependent and prone to overshadowing.

In three experiments, rats were required to find a submerged platform by referring to the boundaries of a circular swimming pool. In the first experiment, rats with lesions of the hippocampus were impaired at finding the hidden platform, lending support for the proposal that learning to find a goal that is a certain direction and distance from a boundary is dependent upon the hippocampus. Experiments 2 and 3 offered preliminary tests to see if such boundary learning occurred incidentally, irrespective of the presence of a reliable landmark. In contrast to this proposal, a landmark hanging above the platform successfully restricted learning about the location of the platform with respect to the boundary of the arena. The discussion explores the capacity of the hippocampus to encode boundary information, as well as interprets the behavioral results on the basis of an associative learning framework.

Rats' orientation is more important than start point location for successful place learning.

Rats were trained to locate food on a plus maze that was moved between 2 locations. The food was in a fixed location relative to room cues but the maze, and the animals' start point, were either translated (shifted to the left or right) or rotated (by 90 degrees or 45 degrees ) across trials. Rats started from the same or different places solved the problem if they headed in a direction different from the start point. Rats started from different places were impaired if they headed in the same direction, suggesting that orientation is more important than start point for successful performance. The same pattern of results was obtained when rats were trained inside a curtained enclosure, suggesting that orientation is not derived solely from a view of distal visual cues while on the maze. It appears that rats use their heading, or direction of movement, to guide their responses at a choice point.

Lesions of the perirhinal cortex do not impair integration of visual and geometric information in rats.

Rats with lesions of the perirhinal cortex and a control group were required to find a platform in 1 corner of a white rectangle and in the reflection of this corner in a black rectangle. Test trials revealed that these groups were able to integrate information regarding the shape of the pool and the color of its walls (black or white) to identify the correct location of the platform. A clear effect of the perirhinal cortex lesions was, however, revealed using an object recognition task that involved the spontaneous exploration of novel objects. The results challenge the view that the perirhinal cortex enables rats to solve discriminations involving feature ambiguity.

A landmark blocks searching for a hidden platform in an environment with a distinctive shape after extended pretraining.

In the blocking phase of three experiments, rats had to find a submerged platform beneath a spherical landmark in one corner of a triangular pool. Prior to this treatment, they were required to find the platform relative to either a sphere above it (blocking groups) or a rod attached to it (control groups). The position of the platform changed from trial to trial for the initial training. The sphere did not restrict learning about the geometric cues provided by the triangular arena in the blocking phase when 12 sessions of initial training took place in either the triangular (Experiment 1) or a circular (Experiment 3) pool. Blocking was observed, however, after 24 sessions of initial training in either the triangular (Experiment 2) or the circular (Experiment 3) pool. Thus, blocking of geometric cues by a landmark is possible after extended initial training with the blocking cue.