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Aged rats need a preserved complement of perforated axospinous synapses per hippocampal neuron to maintain good spatial memory.

Spatial working memory, which crucially depends on the structural integrity of the hippocampal formation and its afferent connections, is impaired in the most, but not all, of aged rats. This study was designed to verify whether aged animals that do not exhibit the spatial memory deficit are the ones in which the hippocampal synaptic connectivity remains preserved with advancing chronological age. Young adult rats with good spatial memory, aged rats with impaired spatial memory and equally aged rats with intact spatial memory were compared. The number of synapses per neuron was estimated in the hippocampal dentate gyrus. The most important results were obtained when axospinous synapses were divided into perforated and non-perforated ones according to the appearance of their postsynaptic density. A significant decrease in the number of perforated synapses was found in memory-impaired aged rats as compared to either young adults or aged animals without memory deficits. The number of non-perforated synapses per neuron was diminished in memory-deficient aged rats relative to young adults, but not to memory-intact aged rats. However, it was only the loss of perforated synapses which correlated with the degree of spatial memory impairment. Thus, aged rats need a preserved complement of hippocampal perforated synapses to maintain good spatial memory.

Aging

Interference in spatial memory.

Four experiments examined interference in human spatial memory. The first two tested for retroactive interference by varying the similarity between the interpolated task and the task that was learned originally. Retroactive interference was observed during relearning of a radial stylus maze and during relearning of the locations of pairs of playing cards in a concentration game. In the third and fourth experiments, proactive interference was tested during the relearning of the locations of pairs in a concentration game. Some proactive interference was observed when the number of proactive games was varied (Experiment 3), and substantial proactive interference was found when the similarity between the proactive and target tasks was the independent variable (Experiment 4). Although extensive evidence indicates that spatial memory differs from other types of memory, spatial memory is subject to interference effects, as are verbal memory, motor memory, visual discriminative memory in animals, and animal spatial memory.

Adult

The effect of culture on a visual-spatial memory task.

The visual-spatial memory ability of 25 Zairian elementary school children was compared with that of 23 Scottish children, using a variation of Kearins's (1976) object placement task. The Scottish children demonstrated significantly better visual-spatial memory than the Zairian children when the easiest (small household objects) of three arrays was presented. The Scottish and Zairian children demonstrated a similar level of visual-spatial ability when the other two arrays (geometric shapes and a variety of natural pieces of wood) were presented, and there were no significant gender differences. Although the Australian Aboriginal children's performance on the visual-spatial task in Drinkwater's (1976) study was superior to the White children's performance (Kearins, 1976, 1981), the Zairian children's performance in this study was not. Perhaps the Aboriginal groups, over countless generations navigating the trackless desert of western Australia, were forced by their environment to develop an aptitude for direction finding that Zairians (whose ecological situation more closely resembles that of Europeans) have not.

Attention

Subjective hierarchies in spatial memory.

Two experiments investigated the structure of spatial memories. Subjects learned locations of objects in spatial layouts (Experiment 1) or locations of object names on maps (Experiment 2). Physical and perceptual boundaries were absent in these spatial arrays. Subjects then participated in three tasks: item recognition, in which the variable of interest was spatial priming; free and cued recall; and Euclidean distance estimation. Ordered-tree analysis of individual subjects' recall protocols produced hierarchical trees consistent with regularities in output order. Spatial priming and distance estimations depended on whether pairs of objects appeared in the same subtree or in different subtrees. These findings indicate that spatial memories have a hierarchical component, even when physical and perceptual boundaries are nonexistent. Priming also increased with depth of clustering in ordered trees. This result supports spreading-activation theories of retrieval but provides evidence against several "non-spreading-activation" theories.

Adult

Differential effects of electroconvulsive shock on concurrent spatial memories: "old" memories are impaired while "new" memories are spared.

The effects of electroconvulsive shock (ECS) on spatial memory first reported by Shavalia, Dodge, and Beatty (1981, Behavioral and Neural Biology, 31, 261-273) were systematically replicated in two experiments. Rats acquired concurrent spatial memories in two 8-arm radial mazes. Each rat was allowed four choices in Maze 1 and then, after 2 h, four choices in Maze 2. After 2 h each rat was tested for retention in Maze 1 and, after 2 more h, was tested for retention in Maze 2. A single ECS was administered immediately after the fourth choice in Maze 2. Retention (as measured by accuracy of Choices 5-8) was diminished for Maze 1 but not for Maze 2. In the second experiment, the delay between the retention tests was eliminated (thus holding the ECS-Choice 5 interval constant for the two mazes). Once again retention of Maze 1 was impaired and retention of Maze 2 was spared; that finding suggests that ECS does not proactively affect radial-arm maze performance. The results of a third experiment converge on the same conclusion; ECS failed to reduce levels of spontaneous alternation. Therefore, ECS appears to interfere retroactively with relatively old spatial memories and newly established memories appear to be immune to the amnestic effects of ECS. Implications and various explanations are considered.

Animals

Spatial memory of children and adults assessed in the radial maze.

To assess the development of accurate spatial memory and its relationship to organized search strategies, children (18-71 months old) and college students searched for rewards hidden at the ends of the arms of an eight-arm radial maze. Subjects made their first four choices in random order selected by the experimenter (forced choice) or in whatever order they wished (free choice). In some conditions, a retention interval was imposed between arm choices 4 and 5, followed by a resumption of the task. With free choice, accuracy of spatial memory increased linearly with age, and the proportion of tests on which the child entered four adjacent arms in sequence during the first four choices, a measure of organized searching, also increased linearly with age. Disrupting this sequential search strategy (forced choice) reduced accuracy for both children and college students, although the reduction with college students was small. Delays had minimal effects for children who met criterion at 0-delay and for college students. Although response patterns seem unimportant in accurate spatial memory in rats, systematic search strategies mature together with, and probably contribute to, the improvement of spatial memory with age in humans.

Adolescent

Sex differences in spatial memory: a reanalysis of block tapping long-term memory according to the short-term memory level.

This paper analyzes the spatial memory performance of 495 subjects. Both short-term and long-term memory have been analyzed by means of the Corsi block-tapping test. We provide separate norms for the learning of a supra-span sequence according to the level of spatial short-term memory. The long-term memory of males and females was compared in groups matched for spatial short-term memory, and the gender effect was never found to be significant. This finding is discussed in relation to the nature of sex differences in spatial abilities.

Educational Status

The development of landmarks in spatial memory: the role of differential experience.

To assess how differential experience with objects in a spatial array might serve to establish relative landmarks within the array, first and fifth graders learned models of a town and farm under two conditions. In a homogeneous condition, all elements in the array were visited an equal number of times. In a landmark condition, the relative landmark status of an element was established by distributing the same total number of visits unequally across the elements. The effects of such landmarks on spatial memory were assessed both in reconstructions of the entire array and by pairwise distance estimations. The landmark condition led to a general improvement in spatial recall accuracy as well as providing a relative landmark within the array to help organize the space. The results suggest that different levels of experience (controlling for overall experience and object salience) can establish elements as relative landmarks in spatial memory. Although there was clear developmental improvement in spatial memory, the specific landmark effects were similar for both first and fifth graders.

Attention

Age-related differences in three-dimensional spatial memory.

This study focused on understanding age differences in spatial memory within a framework relating stimulus qualities to performance. It was hypothesized that elderly adults' spatial memory would be more disadvantaged, relative to young adults, with abstract, meaningless objects than with everyday objects. The study examined differences in memory for the horizontal, vertical, and depth dimensional planes of space in a 4 x 4 x 4 plexiglass cube. College students and community-dwelling adults studied and later reconstructed a three-dimensional arrangement of common or abstract objects located in a compartmentalized cube so that relocation errors could be independently measured within the horizontal, vertical, and depth dimensions. The principal findings were that (a) the magnitude of object displacement in the relocation task was greater for older adults; (b) young and elderly adults differed primarily in terms of large rather than small displacement errors; (c) the locations of meaningless items were more difficult to remember for both age groups; and (d) displacement errors in the vertical dimension were greater than the horizontal and depth dimensions, although this effect was only significant with meaningful items.

Adolescent

The effects of unilateral and bilateral ECT on verbal and visual spatial memory.

Investigated the effects of unilateral left (UL), unilateral right (UR), and bilateral (B) ECT on the performance of right-handed male patients on the Wechsler Memory Scale and two tests of the Williams battery, which provided eight independent measures of verbal memory and two of visual-spatial memory. Patients were tested three times: (1) within 1 week prior to ECT; (2) within 30 minutes after the sixth ECT; (3) 10 days after the sixty ECT. Double blind procedures were maintained carefully. Results showed a significant loss on second testing followed by a significant improvement 10 days later for all ECT groups compared with matched controls. There was some tendency for the UR group to show the least impairment on verbal measures and the UL group to show the least impairment on visual-spatial memory test of the WMS, but most of the differences between UL and UR groups and between each of these and the B group were not significant. The most sensitive test in differentiating among the ECT groups was the brief Verbal Learning subtest of the Williams battery.

Adult

Disproportionate incidental spatial-memory and recall deficits in amnesia.

Seventeen amnesics, including patients with Korsakoff's disease, post-encephalitic amnesia and amnesia caused by rupture of an anterior communicating artery aneurysm, were compared with 17 matched control subjects on a task in which 16 nameable shapes were placed on different squares of a 49-square grid. One version of the task tapped free recall and recognition of the shapes and a second version tapped three forms of spatial memory. The patients were tested after more learning opportunity and shorter delays than were the controls so as to match their recognition levels. Under these conditions, the amnesics performed worse than the controls on free recall, location-to-target memory, target-to-location memory and possibly on non-associative spatial memory although this was less impaired than target-to-location memory. Each of the main aetiological subgroups showed these disproportionate deficits to an apparently similar degree. The disproportionate free recall deficit was unrelated to the spatial memory deficits and overall severity of amnesia, and was associated with ageing and signs of frontal lobe dysfunction. The disproportionate spatial memory deficits were unrelated to frontal lobe dysfunction, but the target-to-location memory measure was associated with impairments of recognition and recall of target material. The results are broadly consistent with the context-memory deficit hypothesis of amnesia.

Adult

Intrahippocampal transplants of septal cholinergic neurons: high-affinity choline uptake and spatial memory function.

Recent studies have demonstrated that intrahippocampal cholinergic septal grafts can ameliorate deficits in spatial memory function and hippocampal cholinergic neurochemical activity in animals with disruptions of the septohippocampal system. However, no study has determined if the restoration of spatial memory function is correlated to the restoration of cholinergic activity, as measured by high-affinity choline uptake (HACU). The present study was designed to determine if such a correlation between behavioral and neurochemical restoration exists. Male Sprague-Dawley rats received either sham lesions (SHAM), bilateral lesions of the septohippocampal pathway (LES), or bilateral lesions along with intrahippocampal septal grafts (SG). After 8 months, rats were tested for their ability to perform spatial reference, spatial navigation and working memory tasks. Upon completion of the behavioral testing, neurochemical activity of the hippocampus was measured by HACU. The results indicate that animals in the SG group had significantly higher behavioral scores and hippocampal HACU rates than animals in the LES group. Regression analysis indicates that a significant correlation exists between performance on each behavioral task and HACU rates. These results demonstrate that hippocampal cholinergic activity, as measured by HACU, correlates significantly with performance on tests of spatial memory function.

Animals

Thalamic role in spatial memory.

The contribution of structures in the limbic diencephalon to spatial memory function was investigated. Rats with lesions of either the anteroventral thalamus, anteromedial thalamus, dorsomedial thalamus or mammillary bodies were compared in their ability to perform a delayed alternation task. The results indicate the ablation of the thalamic nuclei did not impair delayed-alternation memory, but there was impairment following damage to the mammillary bodies. Placement of the discrete lesions was verified using Nissl sections and by tracing the pattern of projections using a silver degeneration stain. The results suggest that individual thalamic nuclei are not essential in the storage and/or retrieval of spatial memory. The data are discussed in terms of spatial deficits resulting from damage to the hippocampus proper or to the pathways connecting it to other brain structures.

Animals

Differential effects of physostigmine and pilocarpine on the spatial memory deficits produced by two septo-hippocampal deafferentations in rats.

Rats that had received two kinds of septo-hippocampal deafferentations, medial septum (MS) lesion and fimbria-fornix (FF) transection, were assayed for brain cholineacetyltransferase (ChAT) activity and spatial memory in an 8-arm radial maze task. Both lesions produced profound and long-lasting spatial memory impairments, which were characterized by a reduction in the numbers of correct arm choices and first correct choices, a reduction in the percent of correct choices and an increase in the number of errors. The degree of memory impairment was severer in FF- than in MS-lesioned rats, and paralleled that of decreases in ChAT activity in the hippocampus. MS lesion reduced ChAT activity in the hippocampus by approximately 45%, while FF lesion almost completely depleted the activity. An intraperitoneal injection of physostigmine (0.0032-0.32 mg/kg), an acetylcholinesterase (AChE) inhibitor, significantly ameliorated the spatial memory deficit induced by MS lesion, but hardly affected that by FF lesion. In contrast, intraperitoneal doses (0.032-3.2 mg/kg) of pilocarpine, a muscarinic agonist, showed a significant improvement of both types of memory deficit with bell shaped dose-response curves. The drug was more potent in the FF- than in the MS-lesioned rats. These results suggest that the septo-hippocampal cholinergic system plays a crucial role in the maintenance of spatial memory, and that the degree of septo-hippocampal deafferentation affects the efficacy of cholinergic drugs.

Animals

Pilocarpine and physostigmine attenuate spatial memory impairments produced by lesions of the nucleus basalis magnocellularis.

The effects of bilateral ibotenic acid-induced lesions of the nucleus basalis magnocellularis (nBM) on the acquisition and retention of several spatial memory tasks were studied in the rat. Maintenance of spatial memory in a food search task was impaired following nBM lesions. Acquisition of spontaneous alternation and reinforced alternation in a T-maze was also significantly impaired in animals with these lesions. In contrast, the animals with nBM lesions were not impaired in the acquisition of a position habit in a T-maze. In several of the tasks there was evidence of some learning in the lesion animals after substantial training, although they were significantly deficient when compared with the controls. Administration of the cholinergic agonists physostigmine sulfate or pilocarpine nitrate prior to behavioral testing resulted in a rapid and significant improvement in the performance of the lesion animals. The ibotenate-induced lesions significantly reduced the activity of choline acetyltransferase (CAT) in the anterior and the posterior neocortex. Hippocampal CAT activity was not changed. The results indicate that the cholinergic projections originating in the nBM are involved in the learning and memory of spatial tasks.

Animals

Spatial memory and adaptive specialization of the hippocampus.

The hippocampus plays an important role in spatial memory and spatial cognition in birds and mammals. Natural selection, sexual selection and artificial selection have resulted in an increase in the size of the hippocampus in a remarkably diverse group of animals that rely on spatial abilities to solve ecologically important problems. Food-storing birds remember the locations of large numbers of scattered caches. Polygynous male voles traverse large home ranges in search of mates. Kangaroo rats both cache food and exhibit a sex difference in home range size. In all of these species, an increase in the size of the hippocampus is associated with superior spatial ability. Artificial selection for homing ability has produced a comparable increase in the size of the hippocampus in homing pigeons, compared with other strains of domestic pigeon. Despite differences among these animals in their histories of selection and the genetic backgrounds on which selection has acted, there is a common relationship between relative hippocampal size and spatial ability.

Adaptation, Physiological

Vasopressin administration via microdialysis into the septum interferes with the acquisition of spatial memory in rats.

The role of vasopressin (AVP) in the septohippocampal system in spatial memory was studied in 27 male hooded rats of the Long-Evans strain. The rats were implanted with a septal microdialysis probe and assigned to 3 groups. Two days later, they were trained on 3 consecutive days (12 daily trials) to locate the hidden underwater platform in the Morris water maze (MWM) while the probes were perfused with either artificial cerebrospinal fluid (aCSF) or aCSF containing vasopressin or the V1 antagonist d(CH2)5Tyr(Me)AVP (AAVP). Another group of rats (n = 8) remained untreated. Groups receiving microdialysis of aCSF or AAVP acquired the MWM task at the same rate as untreated animals. On the other hand, place navigation learning was significantly impaired by microdialysis of AVP during all sessions. The results indicate that endogenous AVP (at least that affecting the V1 receptor subtype) is not indispensable for the acquisition of spatial memories in the MWM, whereas excessive presence of synthetic AVP interferes with spatial learning.

Animals

Preservation of accurate spatial memory in aged rats.

Male rats were tested in an 8 arm radial maze from 6-26 months of age with 5 hr delay imposed between choices 4 and 5. At 26 months their spatial memory was more accurate than when they were first tested at 6 months and also more accurate than that exhibited by another 5 month old group tested concurrently. However, these old rats acquired a noval spatial habit more slowly than the younger animals. In a subsequent study, we compared the acquisition of accurate spatial memory by rats that were 3 or 21.5 months old at the start of training. Older rats adapted to the maze more slowly and required more sessions to achieve criterion with no delay imposed during the test. There was no reliable difference in acquisition when a 1 hr delay was imposed between choices 4 and 5, but the old rats learned more slowly with a 5 hr delay. On memory tests after criterion performance had been achieved, the older rats performed as well as the younger animals at all delay intervals. Aged rats are deficient in acquiring the skills required for accurate spatial memory, but once acquired these skills do not deteriorate. The possibility that other "memory" deficits associated with aging might be alleviated by overtraining is discussed.

Adaptation, Psychological