We tested a densely amnesic patient (P9), with bilateral hippocampal damage resulting from an autoimmune disorder, and 12 age- and sex-matched controls on a series of memory tasks designed to characterize allocentric spatial learning and memory abilities. We compared P9's ability to perform spatial memory tasks with her ability to perform non-spatial, color memory tasks. First, P9's performance was impaired as compared to controls even in the simplest versions of an allocentric spatial memory task, in which she had to find repeatedly over 10 trials the same location(s) of one, two or three illuminating foot pad(s) among 23 pads distributed in an open-field arena. In contrast, she performed as well as controls when she had to find repeatedly over 10 trials the same one, two or three pad(s) marked by color cue(s), whose locations varied between trials. Second, P9's performance was severely impaired in working memory tasks, when she had to learn on a trial-unique basis and remember the location(s) or the color(s) of one, two or three pad(s), while performing an interfering task during the 1-min interval separating encoding and retrieval. Without interference during the retention interval of the trial-unique tasks, P9's performance was partially preserved in the color tasks, whereas it remained severely impaired in the allocentric spatial tasks. Detailed behavioral analyses indicate that P9's memory representations are more limited than those of controls both in their precision (metric coding) and in the number of items that can be maintained in memory (capacity). These findings are consistent with the theory that the hippocampus contributes to the integration or binding of multiple items, in order to produce high-resolution/high-capacity representations of spatial and non-spatial information in the service of short-term/working and long-term memory.

Allocentric spatial memory, the memory for locations coded in relation to objects comprising our environment, is a fundamental component of episodic memory and is dependent on the integrity of the hippocampal formation in adulthood. Previous research from different laboratories reported that basic allocentric spatial memory abilities are reliably observed in children after 2 years of age. Based on work performed in monkeys and rats, we had proposed that the functional maturation of direct entorhinal cortex projections to the CA1 field of the hippocampus might underlie the emergence of basic allocentric spatial memory. We also proposed that the protracted development of the dentate gyrus and its projections to the CA3 field of the hippocampus might underlie the development of high-resolution allocentric spatial memory capacities, based on the essential contribution of these structures to the process known as pattern separation. Here, we present an experiment designed to assess the development of spatial pattern separation capacities and its impact on allocentric spatial memory performance in children from 18 to 48 months of age. We found that: (1) allocentric spatial memory performance improved with age, (2) as compared to younger children, a greater number of children older than 36 months advanced to the final stage requiring the highest degree of spatial resolution, and (3) children that failed at different stages exhibited difficulties in discriminating locations that required higher spatial resolution abilities. These results are consistent with the hypothesis that improvements in human spatial memory performance might be linked to improvements in pattern separation capacities.

Allocentric spatial memory, "where" with respect to the surrounding environment, is one of the three fundamental components of episodic memory: what, where, when. Whereas basic allocentric spatial memory abilities are reliably observed in children after 2 years of age, coinciding with the offset of infantile amnesia, the resolution of allocentric spatial memory acquired over repeated trials improves from 2 to 4 years of age. Here, we first show that single-trial allocentric spatial memory performance improves in children from 3.5 to 7 years of age, during the typical period of childhood amnesia. Second, we show that large individual variation exists in children's performance at this age. Third, and most importantly, we show that improvements in single-trial allocentric spatial memory performance are due to an increasing ability to spatially and temporally separate locations and events. Such improvements in spatial and temporal processing abilities may contribute to the gradual offset of childhood amnesia.

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Cet article résume nos recherches récentes sur l’émergence et le développement typique des capacités de mémoire spatiale allocentrée chez l’enfant. La mémoire spatiale allocentrée est une composante essentielle de la mémoire épisodique, la mémoire des évènements autobiographiques qui se sont passés dans des contextes spatio-temporels uniques. Elle dépend du bon fonctionnement d’une région particulière du cerveau appelée l’hippocampe ou la formation hippocampique. Nos recherches ont montré que la capacité de représentation spatiale allocentrée, intégrant les relations entre différents objets présents dans l’environnement et donc indépendante du point de vue de l’individu, émerge vers l’âge de deux ans. Elle continue de s’améliorer en termes de résolution spatiale et temporelle au cours des cinq à sept années suivantes. L’émergence des capacités de mémoire allocentrée permet également la création de cartes cognitives de l’environnement qui ne dépendent pas de la présence d’information visuelle. Des études neuroanatomiques sur des animaux suggèrent que la maturation de la région CA1 de l’hippocampe contribue à l’émergence d’une mémoire spatiale allocentrée à basse résolution, tandis que la maturation du gyrus denté et de la région CA3 de l’hippocampe contribue à l’amélioration de la mémoire spatiale pendant la petite enfance.