Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-26T03:06:23.643Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  23 July 2013

Shala N. Blue
Affiliation:
Yerkes National Primate Research Center and Department of Psychology, Emory University, Atlanta
Andy M. Kazama
Affiliation:
Yerkes National Primate Research Center and Department of Psychology, Emory University, Atlanta
Jocelyne Bachevalier*
Affiliation:
Yerkes National Primate Research Center and Department of Psychology, Emory University, Atlanta
*
Correspondence and reprint requests to: Jocelyne Bachevalier, Yerkes National Primate Research Center, 954 Gatewood Road, Atlanta, GA 30329. E-mail: jbachev@emory.edu

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. (JINS, 2013, 19, 1–12)

Type
Symposia
Copyright
Copyright © The International Neuropsychological Society 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alvarado, M.C., Bachevalier, J. (2000). Revisiting the development of medial temporal lobe memory functions in primates. Learning & Memory, 7, 244256.CrossRefGoogle ScholarPubMed
Alvarado, M.C., Rudy, J.W. (1995). Rats with damage to the hippocampal-formation are impaired on the transverse-patterning problem but not on elemental discriminations. Behavioral Neuroscience, 109(2), 204211.CrossRefGoogle Scholar
Alvarado, M.C., Wright, A.A., Bachevalier, J. (2002). Object and spatial relational memory in adult rhesus monkeys is impaired by neonatal lesions of the hippocampal formation but not the amygdaloid complex. Hippocampus, 12(4), 421433.CrossRefGoogle Scholar
Bachevalier, J., Beauregard, M. (1993). Maturation of medial temporal lobe memory functions in rodents, monkeys, and humans. Hippocampus, 3(Spec No), 191201.CrossRefGoogle ScholarPubMed
Bachevalier, J., Nemanic, S. (2008). Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex. Hippocampus, 18(1), 6480.CrossRefGoogle ScholarPubMed
Bachevalier, J., Vargha-Khadem, F. (2005). The primate hippocampus: Ontogeny, early insult and memory. Current Opinion in Neurobiology, 15(2), 168174.CrossRefGoogle ScholarPubMed
Bird, C.M., Vargha-Khadem, F., Burgess, N. (2008). Impaired memory for scenes but not faces in developmental hippocampal amnesia: A case study. Neuropsychologia, 46(4), 10501059.CrossRefGoogle Scholar
Blue, S., Kazama, A.M., Bachevalier, J. (2009). The normal development of object-place association memory is altered by neonatal hippocampal lesions in rhesus monkeys. Washington, DC: Society for Neuroscience, Online.Google Scholar
Bullens, J., Nardini, M., Doeller, C.F., Braddick, O., Postma, A., Burgess, N. (2010). The role of landmarks and boundaries in the development of spatial memory. Developmental Science, 13(1), 170180.CrossRefGoogle ScholarPubMed
Burgess, N., Maguire, E.A., O'Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron, 35(4), 625641.CrossRefGoogle ScholarPubMed
Cestari, V., Lucidi, A., Pieroni, L., Rossi-Arnaud, C. (2007). Memory for object location: A span study in children. Canadian Journal of Experimental Psychology, 61(1), 1320.CrossRefGoogle ScholarPubMed
Finger, S., Almli, C.R. (1984). Early brain damage: Neurobiology and behavior (Vol. 2.) Orlando, FL: Academic Press.Google Scholar
Foreman, N., Warry, R., Murray, P. (1990). Development of reference and working spatial memory in preschool children. Journal of General Psychology, 117(3), 267276.Google ScholarPubMed
Gadian, D.G., Aicardi, J., Watkins, K.E., Porter, D.A., Mishkin, M., Vargha-Khadem, F. (2000). Developmental amnesia associated with early hypoxic-ischaemic injury. Brain, 123(Pt 3), 499507.CrossRefGoogle ScholarPubMed
Giedd, J.N., Snell, J.W., Lange, N., Rajapakse, J.C., Casey, B.J., Kozuch, P.L., Rapoport, J.L. (1996). Quantitative magnetic resonance imaging of human brain development: Ages 4–18. Cerebral Cortex, 6(4), 551560.CrossRefGoogle ScholarPubMed
Glavis-Bloom, C., Alvarado, M., Bachevalier, J. (2013). Neonatal hippocampal damage impairs specific food/place associations in adult macaques. Behavioral Neuroscience, 127, 922.CrossRefGoogle ScholarPubMed
Goursaud, A.P., Bachevalier, J. (2007). Social attachment in juvenile monkeys with neonatal lesion of the hippocampus, amygdala and orbital frontal cortex. Behavioral Brain Research, 176(1), 7593.CrossRefGoogle ScholarPubMed
Green, R.J., Stanton, M.E. (1989). Differential ontogeny of working memory and reference memory in the rat. Behavioral Neuroscience, 103(1), 98105.CrossRefGoogle ScholarPubMed
Heuer, E., Bachevalier, J. (2010). Effects of selective neonatal hippocampal lesions on tests of object and spatial recognition memory in monkeys. Behavioral Neuroscience, 125, 137149.CrossRefGoogle Scholar
Hodos, W., Bobko, P. (1984). A weighted index of bilateral brain lesions. Journal of Neuroscience Methods, 12(1), 4347.CrossRefGoogle ScholarPubMed
Jabès, A., Lavenex, P.B., Amaral, D.G., Lavenex, P. (2010). Postnatal development of the hippocampal formation: A stereological study in macaque monkeys. Journal of Comparative Neurology, 519(6), 10511070.CrossRefGoogle Scholar
Jabès, A., Lavenex, P.B., Amaral, D.G., Lavenex, P. (2011). Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus. European Journal of Neuroscience, 31(2), 273285.CrossRefGoogle Scholar
Kazama, A.M., Lay, D., Bachevalier, J. (2003). Delayed maturation of spatial memory in infant monkeys as assessed by a visual paired-comparison task. New Orleans, LA: Society for Neuroscience.Google Scholar
King, J.A., Burgess, N., Hartley, T., Vargha-Khadem, F., O'Keefe, J. (2002). Human hippocampus and viewpoint dependence in spatial memory. Hippocampus, 12(6), 811820.CrossRefGoogle ScholarPubMed
King, J.A., Trinkler, I., Hartley, T., Vargha-Khadem, F., Burgess, N. (2004). The hippocampal role in spatial memory and the familiarity-recollection distinction: A case study. Neuropsychology, 18(3), 405417.CrossRefGoogle ScholarPubMed
Kolb, B., Halliwell, C., Gibb, R. (2010). Factors influencing neocortical development in the normal and injured brain. In M.S. Blumberg, J.H. Freeman, & S.R. Robinson (Eds.), Oxford handbook of developmental behavioral neuroscience. New York: Oxford University Press.Google Scholar
Lavenex, P., Lavenex, P.B. (2006). Spatial relational memory in 9-month-old macaque monkeys. Learning & Memory, 13(1), 8496.CrossRefGoogle ScholarPubMed
Lavenex, P., Lavenex, P. (2009). Spatial memory and the monkey hippocampus: Not all space is created equal. Hippocampus, 19(1), 819.CrossRefGoogle Scholar
Lavenex, P., Lavenex, P.B., Amaral, D.G. (2007). Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys. Nature Neuroscience, 10(2), 234239.CrossRefGoogle ScholarPubMed
Lavenex, P., Lavenex, P.B., Bennett, J.L., Amaral, D.G. (2009). Postmortem changes in the neuroanatomical characteristics of the primate brain: Hippocampal formation. Journal of Comparative Neurology, 512(1), 2751.CrossRefGoogle ScholarPubMed
Lavenex, P.B., Amaral, D.G., Lavenex, P. (2006). Hippocampal lesion prevents spatial relational learning in adult macaque monkeys. Journal of Neuroscience, 26(17), 45464558.CrossRefGoogle ScholarPubMed
Lehnung, M., Leplow, B., Friege, L., Herzog, A., Ferstl, R., Mehdorn, M. (1998). Development of spatial memory and spatial orientation in preschoolers and primary school children. British Journal of Psychology, 89(3), 463480.CrossRefGoogle ScholarPubMed
Leplow, B., Lehnung, M., Pohl, J., Hertzog, A., Ferstl, R., Mehdorn, M. (2003). Navigational place learning in children and young adults as assessed with a standardized locomotor search task. British Journal of Psychology, 94(Pt3), 299317.CrossRefGoogle Scholar
Lenroot, R.H., Giedd, J.N. (2006). Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging. Neuroscience and Biobehavioral Reviews, 30, 718729.CrossRefGoogle ScholarPubMed
Levin, H.S., Grafman, J. (2000). Cerebral reorganization of function after brain damage. New York: Oxford University Press.CrossRefGoogle Scholar
Mahut, H., Moss, M. (1986). The monkey and the seahorse. In R.L. Isaacson & K.H. Pribram (Eds.), The hippocampus. New York: Plenum Press.Google Scholar
Málková, L., Lex, C.K., Mishkin, M., Saunders, R.C. (2001). MRI-based evaluation of locus and extent of neurotoxic lesions in monkeys. Hippocampus, 11(4), 361370.CrossRefGoogle ScholarPubMed
Màlkovà, L., Mishkin, M., Bachevalier, J. (1995). Long-term effects of selective neonatal temporal lobe lesions on learning and memory in monkeys. Behavioral Neuroscience, 109(2), 212226.CrossRefGoogle ScholarPubMed
Mandolesi, L., Petrosini, L., Menghini, D., Addona, F., Vicari, S. (2009). Children's radial arm maze performance as a function of age and sex. International Journal of Developmental Neuroscience, 27(8), 789797.CrossRefGoogle ScholarPubMed
Morris, R.G., Garrud, P., Rawlins, J.N., O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868), 681683.CrossRefGoogle ScholarPubMed
Nadel, L., Hardt, O. (2004). The spatial brain. Neuropsychology, 18(3), 473476.CrossRefGoogle ScholarPubMed
Nardini, M., Burgess, N., Breckenridge, K., Atkinson, J. (2006). Differential developmental trajectories for egocentric, environmental and intrinsic frames of reference in spatial memory. Cognition, 101(1), 153172.CrossRefGoogle ScholarPubMed
Nemanic, S., Alvarado, M.C., Price, R.E., Jackson, E.F., Bachevalier, J. (2002). Assessment of locus and extent of neurotoxic lesions in monkeys using neuroimaging techniques: A replication. Journal of Neuroscience Methods, 121, 199209.CrossRefGoogle ScholarPubMed
Newcombe, N.S., Huttenlocher, J. (2005). Development of spatial cognition. In D. Kuhn & R.S. Siegler (Eds.), Handbook of child psychology (6th ed.). Hoboken, NJ: John Wiley and Sons.Google Scholar
O'Keefe, J., Nadel, L. (1978). The hippocampus as a cognitive map. New York: Oxford University Press.Google Scholar
Overman, W.H., Pate, B.J., Moore, K., Peuster, A. (1996). Ontogeny of place learning in children as measured in the radial arm maze, Morris search task, and open field task. Behavioral Neuroscience, 110(6), 12051228.CrossRefGoogle ScholarPubMed
Pascalis, O., Bachevalier, J. (1999). Neonatal aspiration lesions of the hippocampal formation impair visual recognition memory when assessed by paired-comparison task but not by delayed nonmatching-to-sample task. Hippocampus, 9(6), 609616.3.0.CO;2-A>CrossRefGoogle Scholar
Payne, C., Machado, C.J., Bliwise, N.G., Bachevalier, J. (2010). Maturation of the hippocampal formation and amygdala in Macaca mulatta: A volumetric magnetic resonance imaging study. Hippocampus, 20(8), 922935.CrossRefGoogle ScholarPubMed
Pedhazur, E.J. (1982). Multiple regression in behavioral research: Explanation and prediction (2nd ed.). New York: Holt, Rinehart and Winston.Google Scholar
Pentland, L.M., Anderson, V.A., Dye, S., Wood, S.J. (2003). The Nine Box Maze Test: A measure of spatial memory development in children. Brain & Cognition, 52(2), 144154.CrossRefGoogle ScholarPubMed
Ribordy, F., Jabès, A., Banta Lavenex, P., Lavenex, P. (2012). Development of allocentric spatial memory abilities in children from 18 months to 5 years of age. Cognitive Psychology, 66(1), 129.CrossRefGoogle ScholarPubMed
Rudy, J.W., Stadler-Morris, S., Albert, P. (1987). Ontogeny of spatial navigation behaviors in the rat: Dissociation of “proximal”- and “distal”-cue-based behaviors. Behavioral Neuroscience, 101(1), 6273.CrossRefGoogle ScholarPubMed
Seress, L. (1992). Morphological variability and developmental aspects of monkey and human granule cells: Differences between the rodent and primate dentate gyrus. Epilepsy Research Supplement, 7, 328.Google ScholarPubMed
Seress, L. (2001). Morphological changes of the human hippocampal formation from midgestation to early childhood. In C. Nelson & M. Luciana (Eds.), Handbook of developmental cognitive neuroscience. Cambridge: MIT Press.Google Scholar
Seress, L. (2007). Comparative anatomy of the hippocampal dentate gyrus in adult and developing rodents, non-human primates and humans. Progress in Brain Research, 163, 2341.CrossRefGoogle ScholarPubMed
Seress, L., Abraham, H. (2008). Pre- and postnatal morphological development of the human hippocampal formation. In C. Nelson & M. Luciana (Eds.), Handbook of developmental cognitive neuroscience (2nd ed.). Cambridge: MIT Press.Google Scholar
Seress, L., Ribak, C.E. (1995a). Postnatal development and synaptic connections of hilar mossy cells in the hippocampal dentate gyrus of rhesus monkeys. Journal of Comparative Neurology, 355(1), 93110.CrossRefGoogle ScholarPubMed
Seress, L., Ribak, C.E. (1995b). Postnatal development of CA3 pyramidal neurons and their afferents in the Ammon's horn of rhesus monkeys. Hippocampus, 5(3), 217231.CrossRefGoogle ScholarPubMed
Sluzenski, J., Newcombe, N.S., Satlow, E. (2004). Knowing where things are in the second year of life: Implications for hippocampal development. Journal of Cognitive Neuroscience, 16(8), 14431451.CrossRefGoogle ScholarPubMed
Smith, A.D., Gilchrist, I.D., Cater, K., Ikram, N., Nott, K., Hood, B.M. (2008). Reorientation in the real world: The development of landmark use and integration in a natural environment. Cognition, 107(3), 11021111.CrossRefGoogle Scholar
Spiers, H.J., Burgess, N., Hartley, T., Vargha-Khadem, F., O'Keefe, J. (2001). Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching. Hippocampus, 11(6), 715725.CrossRefGoogle Scholar
von Bonin, G., Bailey, P. (1947). The neocortex of Macaca mulatta. Urbana, IL: University of Illinois Press.Google Scholar
Webster, M.J., Ungerleider, L.G., Bachevalier, J. (1995). Development and plasticity of the neural circuitry underlying visual recognition memory. Canadian Journal of Physiology and Pharmacology, 73, 13641371.CrossRefGoogle ScholarPubMed
Zeamer, A., Bachevalier, J. (2013). Long-term effects of neonatal hippocampal lesions on novelty preference in monkeys. Hippocampus. doi:10.1002/hipo.22139. [Epub ahead of print].CrossRefGoogle ScholarPubMed
Zeamer, A., Heuer, E., Bachevalier, J. (2010). Developmental trajectory of object recognition memory in infant rhesus macaques with and without neonatal hippocampal lesions. Journal of Neuroscience, 30(27), 91579165.CrossRefGoogle ScholarPubMed