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Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys

Nature Neuroscience volume 10, pages 234–239 (2007)Cite this article

Abstract

The hippocampus is important for the acquisition of spatial representations of the environment and consequently in contextual memory. This suggests that the neural substrates underlying spatial cognition might be essential for remembering specific life episodes. Indeed, hippocampal lesions prevent spatial relational learning in adult rodents and monkeys, and result in profound amnesia in adult humans. In contrast, we show here that monkeys with neonatal hippocampal lesions learned new spatial relational information. Our experiments suggest that early hippocampal damage leads to functional brain reorganization that enables spatial information to be acquired through the use of brain regions that normally do not subserve this function.

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Figure 1: Schematic representation of the testing environment and experimental conditions.
Figure 2: Indices of the overall activity level for sham-operated control and hippocampus-lesioned monkeys.
Figure 3: Monkeys' first four choices during standard trials in the local cue condition.
Figure 4: Monkeys' first four choices during standard trials in the spatial relational condition.
Figure 5: Monkeys' choices (all cups that were opened) in the dissociation probe trial (no food present).
Figure 6: Magnetic resonance images showing the medial temporal lobe region in three different section planes (coronal, horizontal and sagittal).
Figure 7: Differential effect of early versus late hippocampal lesions.

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Acknowledgements

We thank J. Bennett and P. Tennant for assistance with surgeries and J. Toscano and J. Burky for assistance with behavioral testing. This research was conducted at the California National Primate Research Center (NIH, base grant RR00169) and was supported by grants from the US National Institute of Health (RO1-NS16980, RO1-MH57502), a Faculty and Alumni Research Development Fund grant from the Department of Psychiatry and Behavioral Sciences at the University of California at Davis and a grant from the Swiss National Science Foundation (PP00A-106701).

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Authors and Affiliations

  1. Department of Psychiatry and Behavioral Sciences, Center for Neuroscience, California National Primate Research Center, The M.I.N.D. Institute, University of California at Davis, 2805 50th St., Sacramento, 95817, California, USA

    Pierre Lavenex, Pamela Banta Lavenex & David G Amaral

  2. Department of Medicine, Unit of Physiology, University of Fribourg, Chemin du Musée 5, Fribourg, CH-1700, Switzerland

    Pierre Lavenex & Pamela Banta Lavenex

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  1. Pierre Lavenex
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  3. David G Amaral
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Correspondence to Pierre Lavenex.

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Supplementary information

Supplementary Figure 1

Magnetic resonance images showing the medial temporal lobe region of experimental monkeys in three different planes of section (coronal, horizontal and sagittal). (PDF 111 kb)

Supplementary Figure 2

Cdk5 Magnetic resonance images showing the medial temporal lobe region of experimental monkeys in three different planes of section (coronal, horizontal and sagittal). (PDF 111 kb)

Supplementary Table 1

First four choices in the spatial relational condition, individual behaviors. (PDF 513 kb)

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Lavenex, P., Lavenex, P. & Amaral, D. Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys. Nat Neurosci 10, 234–239 (2007). https://doi.org/10.1038/nn1820

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