Development of Memory for Spatial Locations and Object/Place Associations in Infant Rhesus Macaques with and without Neonatal Hippocampal Lesions

Abstract

This study traces the development of spatial memory abilities in monkeys and reports the effects of selective neonatal hippocampal lesions on performance across development. Two different versions of the visual paired-comparison (VPC) task were used. The VPC-Spatial-Location task tested memory for object-locations that could be solved using an egocentric spatial frame of reference and the VPC-Object-In-Place task taxed memory for spatial relations using an allocentric reference frame. Eleven rhesus macaques (6 neonatal sham-operated controls and 5 with neonatal neurotoxic hippocampal lesions) were tested on both tasks as infants (8 months), juveniles (18 months), and adults (5–6 years). Memory for spatial locations was present by 18 months of age, whereas memory for object-place relations was present only in adulthood. Also, neonatal hippocampal lesions delayed the emergence of memory for spatial locations and abolished memory for object-place associations, particularly in animals that had sustained extensive and bilateral hippocampal lesions. The differential developmental time course of spatial memory functions and of the effects of neonatal hippocampal lesions on these functions are discussed in relation to morphological maturation of the medial temporal lobe structures in monkeys. Implications of the findings for the neural basis of spatial memory development in humans are also considered.

What goes where? Eye tracking reveals spatial relational memory during infancy

“…Although orientation using landmarks begins to emerge within the first year (Acredolo & Evans, 1980;Lew, Bremner, & Lefkovitch, 2000), the ability to use the relations between multiple distal cues is not seen until at least 24 months of age (Newcombe, Huttenlocher, Drummey, & Wiley, 1998;Ribordy et al, 2013). Blue et al (2013) argued that visual Fig. 4.…”

“…Thus, by measuring eye movements directly, we are able to measure memory processes without the challenge of controlling for age-related differences in gross motor behavior. The procedure is adapted from the VPC task used by Bachevalier and Nemanic (2008), Blue et al (2013); however, children were tested with single-object arrays rather than pairs of novel and familiar arrays. Children were familiarized with displays of three objects in a triangular spatial configuration (top left, top right, and bottom middle).…”

“…The results showed that monkeys with hippocampal lesions exhibited novelty preferences when tested with object arrays containing novel items but exhibited null preferences when tested with arrays in which the identity of the objects remained the same but their relative position had changed. Blue, Kazama, and Bachevalier (2013) recently looked at the development of spatial relational memory in monkeys tested on the same task at 8 months, at 18 months, and as adults (5-6 years). In control animals, novelty preferences on this task increased with age; however, animals that had received neonatal hippocampal lesions exhibited null preferences at all ages.…”

“…In control animals, novelty preferences on this task increased with age; however, animals that had received neonatal hippocampal lesions exhibited null preferences at all ages. The ability to learn about spatial relations among an array of objects has a relatively protracted developmental trajectory and depends on the integrity of the hippocampus in monkeys (Bachevalier & Nemanic, 2008;Blue et al, 2013).…”

Memory for complex visual objects but not for allocentric locations during the first year of life

“…This procedure makes possible the examination of allocentric memory by manipulating the object arrangements during the test phase (spatial version of the VPC task). So far, the spatial VPC task has been used in Monkeys (Bachevalier & Nemanic, 2008;Blue, Kazama, & Bachevalier, 2013) and rats (Wan, Aggleton, & Brown, 1999), and has shown recognition memory for familiarized arrangements in adult animals, but not earlier in development.…”