Dissociable spatial memory systems revealed by typical and atypical human development

Abstract

Rodent lesion studies have revealed the existence of two causally dissociable spatial memory systems, localized to the hippocampus and striatum that are preferentially sensitive to environmental boundaries and landmark objects, respectively. Here we test whether these two memory systems are causally dissociable in humans by examining boundary- and landmark-based memory in typical and atypical development. Adults with Williams syndrome (WS)-a developmental disorder with known hippocampal abnormalities-and typical children and adults, performed a navigation task that involved learning locations relative to a boundary or a landmark object. We found that boundary-based memory was severely impaired in WS compared to typically-developing mental-age matched (MA) children and chronological-age matched (CA) adults, whereas landmark-based memory was similar in all groups. Furthermore, landmark-based memory matured earlier in typical development than boundary-based memory, consistent with the idea that the WS cognitive phenotype arises from developmental arrest of late maturing cognitive systems. Together, these findings provide causal and developmental evidence for dissociable spatial memory systems in humans.

A Critical Review of Spatial Abilities in Down and Williams Syndromes: Not All Space Is Created Equal

“…Response learning has been shown to be facilitated in the presence of hippocampal dysfunction (9). In our response learning task, individuals with DS and individuals with WS exhibited better performance than MA-matched TD children, suggesting that the neurobiological substrates subserving response learning are relatively intact in these two syndromes and that impaired hippocampal function contributes to improved performance in striatal-dependent tasks in these individuals (36,37,70).…”

The Development of Human Cortical Scene Processing

“…If OPA supports visually guided navigation and matures late in childhood, then we should also predict that children's visually guided navigation abilities to mature late in development. Consistent with this idea, a recent study investigated the development of spatial memory relative to boundaries using a task known to depend on OPA by adulthood ( Julian et al, 2016) and found protracted development late into childhood ( Julian et al, 2019). Furthermore, unlike adults, younger children are poorer at utilizing peripheral cues while navigating (Franchak & Adolph, 2010) and make more errors in obstacle avoidance and path-following tasks (Berard & Vallis, 2006).…”

“…Third, and finally, the limited available evidence nevertheless supports the idea of protracted development of visually guided navigation. For example, as alluded to earlier, navigation-related skills, including locomotion (Franchak & Adolph, 2010), obstacle avoidance (Berard & Vallis, 2006), and boundary-based spatial memory (Julian et al, 2019), appear to undergo protracted developmental trajectories, still developing as late as 8 years old. By contrast, scene recognition abilities appear early in life—even infants can recognize scene information (i.e., discriminating whether a cliff is deep or shallow) long before they can independently move around their surroundings (e.g., by crawling; Campos et al, 1970).…”

Late Development of Navigationally Relevant Motion Processing in the Occipital Place Area

“…To study how navigationally relevant information processing develops in the occipital place area (OPA), we measured responses in OPA across childhood to first-person perspective motion-a proxy for the visual experience of actually navigating through an immediately visible scene. Given previous findings that boundary-based navigation and other dorsal stream processes are still developing in childhood [14][15][16], we scanned two groups of children: 5 year olds and 8 year olds. Responses in OPA were measured using functional magnetic resonance imaging (fMRI) while participants viewed (1) 3-s video clips of firstperson perspective motion through scenes (''dynamic scenes''), mimicking the actual visual experience of visually guided navigation, and (2) 3 1-s still images taken from these same video clips, rearranged such that first-person perspective motion could not be inferred (''static scenes'').…”