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. 2013 Nov;19(10):1053-64.
doi: 10.1017/S1355617713000799. Epub 2013 Jul 23.

Development of memory for spatial locations and object/place associations in infant rhesus macaques with and without neonatal hippocampal lesions

Shala N Blue  1 , Andy M Kazama, Jocelyne Bachevalier
Affiliations

Development of memory for spatial locations and object/place associations in infant rhesus macaques with and without neonatal hippocampal lesions

Shala N Blue et al. J Int Neuropsychol Soc. 2013 Nov.

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.

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Conflict of interest statement

We acknowledge that none of the authors have a conflict of interest with the publication of this manuscript.

Figures

Fig. 1
Fig. 1
Examples of trials for the visual paired-comparison (VPC) -Spatial-Location (A), VPC-Object-In-Place (B), and VPC-Object-Control (C) tasks. Note that for the Spatial-Location task, the novel image is the same as the familiar image but is placed in a different position on the screen. For the Object-In-Place tasks, the novel image differed from the familiar image only in the location of three of the five objects forming the images (black arrows). In the Object-Control task, the novel image consisted of replacing three objects of the familiar image with three new objects (black arrows).
Fig. 2
Fig. 2
High-resolution T1 images at three levels of the hippocampal formation in a sham-operated animal (case Neo-C-1, right hemisphere) and in an animal with neonatal hippocampal lesions (case Neo-Hibo-2, left and right hemispheres) taken when the animals were 1–2 years of age. Note the almost complete loss of hippocampal tissue in this case.
Fig. 3
Fig. 3
Mean percent of time (± SEM) looking at the familiar object appearing in the novel location in the visual paired-comparison (VPC) -Spatial-Location task (A) and at the novel image in the VPC-Object-In-Place (B) and VPC-Object-Control (C) tasks for animals with neonatal sham operations (Group Neo-C, white bars) and animals with neonatal hippocampal lesions (Group Neo-Hibo, black bars). Animals were tested at 8 months, 18 months, and 5–6 years of age for the 3 tasks. Note that for the VPC-Spatial-Location at 18 months and the VPC-Object-In-Place at 5–6 years when novelty preference did not differ from chance, white circles illustrate scores of two animals with bilateral hippocampal lesions, whereas black circles illustrate scores of the 3 animals with mostly unilateral hippocampal lesions (see Table 1). The horizontal dashed line represents chance performance and asterisk indicates significant difference from chance (p < .05).
Fig. 4
Fig. 4
Mean percent of time (± SEM) looking at the novel image in the visual paired-comparison (VPC) -Spatial-Location task (A) and VPC-Object-In-Place task (B) for adult animals with sham operations (white bars) and animals with hippocampal lesions (black bars). Neo-lesion represents adult animals with infant-onset lesions and Ad-lesion represents adult animals with adult-onset lesions. Conventions as in Figure 3.
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