Neurons sensitive to both place and direction from distinct regions of the hippocampal formation, allometric relationships between spatial learning and hippocampal structure and pronounced impairments in spatial learning after lesions in this area, indicate that the hippocampal formation subserves allocentric spatial learning. To learn more about the process of spatial representation, we have developed a task that provides independent control of both landmark and directional cues. On the basis of physiological and behavioural work, this task also makes it possible to investigate the relevance of associative learning principles, such as predictability, to the spatial domain. We report here that although rats learn to discriminate between landmarks on the basis of their proximity to a reliably predicted food reward, they will only learn to use them to represent its location if they maintain stable locations within a geometric frame of reference.
Volumetric studies in a range of animals (London taxi-drivers, polygynous male voles, nest-parasitic female cowbirds, and a number of food-storing birds) have shown that the size of the hippocampus, a brain region essential to learning and memory, is correlated with tasks involving an extra demand for spatial learning and memory. In this paper, we report the quantitative advantage that food storers gain from such an enlargement. Coal tits (Parus ater) a food-storing species, performed better than great tits (Parus major), a nonstoring species, on a task that assessed memory persistence but not on a task that assessed memory resolution or on one that tested memory capacity. These results show that the advantage to the food-storing species associated with an enlarged hippocampus is one of memory persistence. There are at least three constituent aspects to spatial learning and memory: memory capacity (the number of locations remembered), memory persistence (the duration over which a location is remembered), and spatial resolution (the least distance at which remembered locations can be discriminated). Although volumetric studies have shown that several behavioral adaptations are associated with an enlarged hippocampus (1-6), no volumetric study, nor any of a number of experiments examining spatial memory performance (7-16), has yet been able to determine whether the observed enlargement of the hippocampus in food-storing and other species is associated with one, two, or all three of these aspects of memory. If food-storers have a greater memory capacity than the nonstorers, we predict that performance would be similar when there is only one item to remember, but would diverge with increasing number of items, with the nonstorers having a poorer performance when required to remember more items (see Fig. 1A). If the species differed only in the spatial resolution of memory, they should achieve similar performance levels when items are far apart, but the food storers should perform better when the items are close together (Fig. 1B). If the food storers only have a longer-lasting memory, then the species difference in performance should be similar regardless of number of items or their proximity ( Fig. 1C; see ref. 17 for a similar argument).In this experiment, wild-caught food storers [coal tits (Parus ater), a species with an enlarged hippocampus] and a related nonstoring species [great tits (Parus major)] were tested on all of these three aspects of spatial memory within the same experiment. All birds were presented with one to four white squares on a computer-controlled touch screen. Squares disappeared after a peck was directed at them. Once all squares had been pecked and after a retention interval, the birds were presented with a square in one of these earlier locations and a second square in a new location. They were rewarded for pecking the square in the new location (the ''target''), following a spatial nonmatching rule. Memory capacity was tested by varying the number of sample images to be remembered from on...
A characteristic feature of associative conditioning is that learning a predictive relationship between two events can block later learning about an added event. It is not yet well established whether blocking occurs in the spatial domain or the circumstances in which it does. We now report, using rats trained to search for hidden food near landmarks in an open field arena, that blocking can occur in spatial learning. The animals noticed the added landmark at the start of the blocking phase and explored it, but either failed to incorporate it into their spatial map or developed a representation in which only some landmarks actually control behavior. Additionally, performance at asymptote was controlled by the shape of the landmark array rather than the individual landmarks comprising it, indicating that blocking in the spatial domain may represent a failure to alter the encoded geometry of a learned array.
Uncertainty plays an important role in several navigational computations. Navigation typically depends on multiple sources of information, and different navigational systems may operate both in parallel and in combination. The optimal combination of information from different sources must take into account the uncertainty of that information. We distinguish between two types of spatial uncertainty, precision, and reliability. Precision is the inverse variance of the probability distribution that describes the information a cue contributes to an organism's knowledge of its location. Reliability is the probability of the cue being correctly identified, or the probability of a cue being related to a target location. We argue that in most environments, precision and reliability are negatively correlated. In case of cue conflict, precision and reliability must be traded off against each other. We offer a quantitative description of optimal behaviour. Knowledge of uncertainty is also needed to optimally determine the point where a search should start when an organism has more precise spatial information in one of the spatial dimensions. We show that if there is any cost to travel, it is advantageous to head off to one side of the most likely target location and head toward the target. The magnitude of the optimal offset depends on both travel cost and search cost.
To investigate whether spatial learning complies with associative learning theories or with theories of cognitive mapping, rats were trained in three experiments exploring the effect of variations in spatial predictive relationships. In experiment 1, it was found that making one of two landmarks the sole spatial predictor of reward, by varying the spatial relationship between reward and other cues, reduced the control over search exerted by that landmark compared with that observed when the landmark and context cues were both reliable predictors of reward location. This requirement for landmark stability rather than predictive power appears to contradict results obtained in conventional conditioning paradigms. Discrimination learning was unaffected, suggesting a dissociation between discrimination and spatial learning with respect to the influence of geometric stability. Further experiments used arrays of both single and multiple landmarks. Experiment 2 revealed that the stability of a single landmark improved accuracy of search, but also showed that local stability between a pair of landmarks that moved around the arena together was sufficient to support spatial learning. Experiment 3 examined landmark stability using fixed directional cues in the absence of vestibular disorientation. This also revealed a relative advantage of stable landmarks, but animals presented with a landmark that moved from trial to trial did show some evidence of learning. Parametric manipulation of landmark stability offers an intriguing way of influencing the process of spatial representation and thus understanding better the processes through which egocentric representations of perceived space are transformed into allocentric representations of the real world.
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