Improvement of allocentric spatial memory resolution in children from 2 to 4 years of age

Abstract

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.

Commentary

“…Our recent work at the genetic and neuroanatomical levels revealed that different hippocampal regions mature at different times during development (Favre, Banta Lavenex, & Lavenex, 2012a, 2012bJabès, Banta Lavenex, Amaral, & Lavenex, 2010Lavenex, Banta Lavenex, & Amaral, 2007;Lavenex, Sugden, Davis, Gregg, & Banta Lavenex, 2011). These findings, together with our studies of the development of human spatial memory (Ribordy, Jabès, Banta Lavenex, & Lavenex, 2013;Ribordy Lambert, Lavenex & Banta Lavenex, 2015), support the hypothesis that the differential maturation of distinct hippocampal circuits might underlie the differential emergence of specific ''hippocampus-dependent'' memory processes, culminating in the emergence of adult-like episodic memory concomitant with the maturation of all hippocampal circuits . This is a view shared by Jabès and Nelson (2015).…”

Dissociation of spatial memory systems in Williams syndrome

“…Indeed, 70% of the indivuals with WS that we tested were incapable of solving our task, which can be considered the most basic of place (Ribordy, Jabes, Banta Lavenex, & Lavenex, 2013;Ribordy Lambert, Lavenex, & Banta Lavenex, 2015).…”

The “when” and the “where” of single‐trial allocentric spatial memory performance in young children: Insights into the development of episodic memory

“…The offset of infantile amnesia, when children become capable of long-term encoding of some, albeit few, episodic memories, occurs around 2 years of age (Newcombe et al, 2007;Rubin, 2000). Similarly, basic allocentric spatial memory abilities are reliably observed in children after 2 years of age (Newcombe, Huttenlocher, Bullock Drummey, & Wiley, 1998;Ribordy et al, 2013, Ribordy Lambert et al, 2015.…”

“…In a series of experiments by Ribordy et al (2013) and Ribordy Lambert et al (2015), children were asked to find rewards hidden beneath cups in an open-field arena, over repeated trials. The simplest version of this task required children to learn and remember one rewarded location among four potentially rewarded locations.…”

“…From 42 months of age, children were capable of discriminating locations above chance level (Ribordy et al, 2013). In a third experiment, the same authors tested children between 18-and 48-months of age over a 4-week period on a series of spatial tasks in which the distance between the potentially rewarded locations decreased, and the number of rewarded and potentially rewarded locations increased, from week to week (Ribordy Lambert et al, 2015). This experiment confirmed that allocentric spatial memory capacities improve from 2 to 4 years of age, and showed that children that failed at successive stages exhibited difficulty in discriminating locations that required high spatial resolution, also known as spatial pattern separation abilities, a process known to be subserved by the hippocampal formation (Bakker et al, 2008;Gilbert et al, 2001).…”