Spatial Relational Learning Research Articles

Functional organization of the medial temporal lobe memory system following neonatal hippocampal lesion in rhesus monkeys.

Hippocampal damage in adult humans impairs episodic and semantic memory, whereas hippocampal damage early in life impairs episodic memory but leaves semantic learning relatively preserved. We have previously shown a similar behavioral dissociation in nonhuman primates. Hippocampal lesion in adult monkeys prevents allocentric spatial relational learning, whereas spatial learning persists following neonatal lesion. Here, we quantified the number of cells expressing the immediate-early gene c-fos, a marker of neuronal activity, to characterize the functional organization of the medial temporal lobe memory system following neonatal hippocampal lesion. Ninety minutes before brain collection, three control and four adult monkeys with bilateral neonatal hippocampal lesions explored a novel environment to activate brain structures involved in spatial learning. Three other adult monkeys with neonatal hippocampal lesions remained in their housing quarters. In unlesioned monkeys, we found high levels of c-fos expression in the intermediate and caudal regions of the entorhinal cortex, and in the perirhinal, parahippocampal, and retrosplenial cortices. In lesioned monkeys, spatial exploration induced an increase in c-fos expression in the intermediate field of the entorhinal cortex, the perirhinal, parahippocampal, and retrosplenial cortices, but not in the caudal entorhinal cortex. These findings suggest that different regions of the medial temporal lobe memory system may require different types of interaction with the hippocampus in support of memory. The caudal perirhinal cortex, the parahippocampal cortex, and the retrosplenial cortex may contribute to spatial learning in the absence of functional hippocampal circuits, whereas the caudal entorhinal cortex may require hippocampal output to support spatial learning.

A consistent but non-coincident visual pattern facilitates the learning of spatial relations among locations

Human participants searched in a dynamic three-dimensional computer-generated virtual-environment open-field search task for four hidden goal locations arranged in a diamond configuration located in a 5 × 5 matrix of raised bins. Participants were randomly assigned to one of two groups: visual pattern or visual random. All participants experienced 30 trials in which four goal locations maintained the same spatial relations to each other (i.e., a diamond pattern), but this diamond pattern moved to random locations within the 5 × 5 matrix from trial to trial. For participants in the visual pattern group, four locations were marked in a distinct color and arranged in a diamond pattern that moved to a random location independent of the hidden spatial pattern from trial to trial throughout the experimental session. For participants in the visual random group, four random locations were marked with a distinct color and moved to random locations independent from the hidden spatial pattern from trial to trial throughout the experimental session. As a result, the visual cues for the visual pattern group were consistent but not coincident with the hidden spatial pattern, whereas the visual cues for the visual random group were neither consistent nor coincident with the hidden spatial pattern. Results indicated that participants in both groups learned the spatial configuration of goal locations and that the presence of consistent but noncoincident visual cues facilitated the learning of spatial relations among locations.

No evidence that consistent auditory cues facilitate learning of spatial relations among locations

Human participants searched in a dynamic three-dimensional computer-generated virtual-environment open-field search task for four hidden goal locations arranged in a diamond configuration located in a 5×5 matrix of raised bins. Participants were randomly assigned to one of two groups: Consistent or Inconsistent. All participants experienced 30 trials in which four goal locations maintained the same spatial relations to each other (i.e., a diamond pattern), but this diamond pattern moved to random locations within the 5×5 matrix from trial-to-trial. For participants in the Consistent group, each goal location within the pattern always provided a unique and consistent auditory cue throughout the experimental session. For participants in the Inconsistent group, the same distinct auditory cues were provided for each goal location; however, the locations of these auditory cues within the pattern itself were randomized from trial-to-trial throughout the experimental session. Results indicated that participants in both groups learned the spatial configuration of goal locations, but the presence of consistent auditory cues did not facilitate the learning of spatial relations among locations.

A Common Frame of Reference for Learned and Communicated Vectors in Honeybee Navigation

Humans draw maps when communicating about places or verbally describe routes between locations. Honeybees communicate places by encoding distance and direction in their waggle dances. Controversy exists not only about the structure of spatial memory but also about the efficiency of dance communication. Some of these uncertainties were resolved by studies in which recruits' flights were monitored using harmonic radar. We asked whether the two sources of vector information--the previously learned flight vector to a food source and the communicated vector--are represented in a common frame of spatial reference. We found that recruits redirect their outbound flights and perform novel shortcut flights between the communicated and learned locations in both directions. Guidance by beacons at the respective locations or by the panorama of the horizon was excluded. These findings indicate a spatial reference based on either large-scale vector integration or a common geocentric map-like spatial memory. Both models predict a memory structure that stores the spatial layout in such a way that decisions are made according to estimated distances and directions. The models differ with respect to the role of landmarks and the time of learning of spatial relations.

Spatial relational learning and memory abilities do not differ between men and women in a real-world, open-field environment

This study assesses gender differences in spatial and non-spatial relational learning and memory in adult humans behaving freely in a real-world, open-field environment. In Experiment 1, we tested the use of proximal landmarks as conditional cues allowing subjects to predict the location of rewards hidden in one of two sets of three distinct locations. Subjects were tested in two different conditions: (1) when local visual cues marked the potentially-rewarded locations, and (2) when no local visual cues marked the potentially-rewarded locations. We found that only 17 of 20 adults (8 males, 9 females) used the proximal landmarks to predict the locations of the rewards. Although females exhibited higher exploratory behavior at the beginning of testing, males and females discriminated the potentially-rewarded locations similarly when local visual cues were present. Interestingly, when the spatial and local information conflicted in predicting the reward locations, males considered both spatial and local information, whereas females ignored the spatial information. However, in the absence of local visual cues females discriminated the potentially-rewarded locations as well as males. In Experiment 2, subjects (9 males, 9 females) were tested with three asymmetrically-arranged rewarded locations, which were marked by local cues on alternate trials. Again, females discriminated the rewarded locations as well as males in the presence or absence of local cues. In sum, although particular aspects of task performance might differ between genders, we found no evidence that women have poorer allocentric spatial relational learning and memory abilities than men in a real-world, open-field environment.

Spatial memory and the monkey hippocampus: Not all space is created equal

Studies of the role of the monkey hippocampus in spatial learning and memory, however few, have reliably produced inconsistent results. Whereas the role of the hippocampus in spatial learning and memory has been clearly established in rodents, studies in nonhuman primates have made a variety of claims that range from the involvement of the hippocampus in spatial memory only at relatively longer memory delays, to no role for the hippocampus in spatial memory at all. In contrast, we have shown that selective damage restricted to the hippocampus (CA regions) prevents the learning or use of allocentric, spatial relational representations of the environment in freely behaving adult monkeys tested in an open-field arena. In this commentary, we discuss a unifying framework that explains these apparently discrepant results regarding the role of the monkey hippocampus in spatial learning and memory. We describe clear and strict criteria to interpret the findings from previous studies and guide future investigations of spatial memory in monkeys. Specifically, we affirm that, as in the rodent, the primate hippocampus is critical for spatial relational learning and memory, and in a time-independent manner. We describe how claims to the contrary are the result of experimental designs that fail to recognize, and control for, egocentric (hippocampus-independent) and allocentric (hippocampus-dependent) spatial frames of reference. Finally, we conclude that the available data demonstrate unequivocally that the central role of the hippocampus in allocentric, spatial relational learning and memory is conserved among vertebrates, including nonhuman primates.

Quantitative and qualitative sex differences in spatial navigation

We examined sex differences in spatial navigation performance using an ecologically relevant experimental paradigm in which virtual maze-like museums are projected in front of a treadmill. Thirty-two 20-30-year-old adults (16 women/16 men) performed a way-finding task in city-block (straight corridors) or variable (irregular corridors) topographies while walking on the treadmill. Sex differences in spatial navigation performance were reduced in variable topographies, suggesting less reliance on spatial relational learning among women. Also, spatial geometric knowledge of the mazes continued to be higher in men after all participants had attained perfect place-finding performance. Results indicate that sex differences in spatial navigation performance are modulated by interactions between environmental demands and sex differences in spatial processing.

Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys

The hippocampus is important for the acquisition of spatial representations of the environment and consequently in contextual memory. This suggests that the neural substrates underlying spatial cognition might be essential for remembering specific life episodes. Indeed, hippocampal lesions prevent spatial relational learning in adult rodents and monkeys, and result in profound amnesia in adult humans. In contrast, we show here that monkeys with neonatal hippocampal lesions learned new spatial relational information. Our experiments suggest that early hippocampal damage leads to functional brain reorganization that enables spatial information to be acquired through the use of brain regions that normally do not subserve this function.

Spatial relational learning in rufous hummingbirds (Selasphorus rufus)

There is increasing evidence that animals can learn abstract spatial relationships, and successfully transfer this knowledge to novel situations. In this study, rufous hummingbirds (Selasphorus rufus) were trained to feed from either the lower or the higher of two flowers. When presented with a test pair of flowers, one of which was at a novel height, they chose the flower in the appropriate spatial position rather than the flower at the correct height. This response may also have been influenced by a preference for taller flowers as acquisition of the task during experimental training occurred more readily when the reward flower was the taller of the pair. Thus, it appears that although learning abstract relationships may be a general phenomenon across contexts, and perhaps across species, the ease with which they are learned and the context in which they are subsequently used may not be the same.

Hippocampal Lesion Prevents Spatial Relational Learning in Adult Macaque Monkeys

The role of the hippocampus in spatial learning and memory has been extensively studied in rodents. Comparable studies in nonhuman primates, however, are few, and findings are often contradictory. This may be attributable to the failure to distinguish between allocentric and egocentric spatial representations in experimental designs. For this experiment, six adult monkeys received bilateral hippocampal ibotenic acid lesions, and six control subjects underwent sham surgery. Freely moving monkeys then foraged for food located in two arrays of three distinct locations among 18 locations distributed in an open-field arena. Multiple goals and four pseudorandomly chosen entrance points precluded the monkeys' ability to rely on an egocentric strategy to identify food locations. Monkeys were tested in two conditions. First, local visual cues marked the food locations. Second, no local cues marked the food locations, so that monkeys had to rely on an allocentric (spatial relational) representation of the environment to discriminate these locations. Both hippocampal-lesioned and control monkeys discriminated the food locations in the presence of local cues. However, in the absence of local cues, control subjects discriminated the food locations, whereas hippocampal-lesioned monkeys were unable to do so. Interestingly, histological analysis of the brain of one control monkey whose behavior was identical to that of the experimentally lesioned animals revealed a bilateral ischemic lesion restricted to the hippocampus. These findings demonstrate that the adult monkey hippocampal formation is critical for the establishment or use of allocentric spatial representations and that selective damage of the hippocampus prevents spatial relational learning in adult nonhuman primates.

Environmental topography and postural control demands shape aging-associated decrements in spatial navigation performance.

This study tests the hypothesis that aging-induced cognitive permeation of sensorimotor functions contributes to adult age differences in spatial navigation performance. Virtual maze-like museums were projected in front of a treadmill. Sixteen 20-30-year-old men and sixteen 60-70-year-old men performed a way-finding task in city-block or variable topographies while walking with or without support. Walking support attenuated age-related decrements in navigational learning. Navigation load increased trunk-angle variability for older adults only. Age differences in spatial knowledge persisted despite perfect place-finding performance. City-block topography was easier than variable topography for younger adults only, indicating age-related differences in reliance on spatial relational learning. Attempts at supporting older adults' navigation performance should consider sensorimotor/cognitive interactions and qualitative differences in navigational activity.

Object and spatial relational memory in adult rhesus monkeys is impaired by neonatal lesions of the hippocampal formation but not the amygdaloid complex.

Adult rhesus monkeys with neonatal aspiration lesions of the hippocampal formation or the amygdaloid complex (including their respective subjacent cortices) and their age-matched controls were tested on the transverse patterning problem (A+ vs. B-, B+ vs. C- and C+ vs. A-) and a spatial version of the delayed nonmatching-to-sample (DNMS) task with delays of 10 s to 30 s, 60 s, 120 s, and 600 s. Monkeys with neonatal damage to the amygdaloid complex learned both tasks and did not differ from controls at any delay of the spatial DNMS task. Monkeys with neonatal hippocampal damage, however, were unable to learn transverse patterning, though they easily transferred to a linear series (A+ vs. B-, B+ vs. C-, and C+ vs. X-). Three of the four were also unable to reach criterion on the spatial DNMS task within the limits of testing, and the performance of all four monkeys deteriorated with increasing choice delays. The data suggest a role of the primate hippocampal region in both object and spatial relational learning.

Exploration and learning of topographical relationships by the rat

In three experiments, the exploratory behavior of thirsty rats systematically progressed to areas distant from the starting location in an unfamiliar environment (table with seven objects on it). In a fourth experiment, this systematic pattern was disrupted when one of the objects in the new environment was familiar. Learning of spatial relations occurred during exploration, as evidenced by exploratory behavior on a test in which a previously neutral object in the environment became a source of water. Exploratory activity differed when the starting location was fixed in one corner of the table from when it was varied daily from corner to corner on a large table in one experiment; it did not differ with a table half that size in another experiment. The findings are taken to indicate that the development of the spatial structure consists of utilizing a known part of a given locale as anchor point or “base of operations” upon which is built a network of topographic relations among objects in particular locales.

Effects of early and late blindness on auditory spatial learning in the rat

Animals which had been peripherally blinded by enucleation shortly after birth were found to perform significantly more poorly on an auditory localization task than those blinded in a similar manner at 90 days of age. A subsequent experiment demonstrated that those animals which had been blinded early in life tended to perform better than late-blinded animals on a non-spatial auditory learning task. The results are interpreted as demonstrating a deficit in learning of spatial relations in the early-blind.