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Age does not increase rate of forgetting over weeks—Neuroanatomical volumes and visual memory across the adult life-span

Published online by Cambridge University Press:  28 January 2005

ANDERS M. FJELL ,
KRISTINE B. WALHOVD ,
IVAR REINVANG ,
ARVID LUNDERVOLD ,
ANDERS M. DALE ,
BRIAN T. QUINN ,
NIKOS MAKRIS  and
BRUCE FISCHL
ANDERS M. FJELL
Affiliation:
Institute of Psychology, University of Oslo, Oslo, Norway
KRISTINE B. WALHOVD
Affiliation:
Institute of Psychology, University of Oslo, Oslo, Norway
IVAR REINVANG
Affiliation:
Institute of Psychology, University of Oslo, Oslo, Norway Department of Psychosomatic Medicine, Rikshospitalet University Hospital, Oslo, Norway
ARVID LUNDERVOLD
Affiliation:
Department of Physiology & Locus on Neuroscience, University of Bergen, Bergen, Norway
ANDERS M. DALE
Affiliation:
MGH-NMR Center, Massachusetts General Hospital, Harvard University, Cambridge, Massachusetts MR Center, Norwegian University of Science and Technology, Trondheim, Norway Departments of Neurosciences and Radiology, University of California, San Diego
BRIAN T. QUINN
Affiliation:
MGH-NMR Center, Massachusetts General Hospital, Harvard University, Cambridge, Massachusetts
NIKOS MAKRIS
Affiliation:
Center for Morphometric Analysis, Massachusetts General Hospital, Harvard University, Cambridge, Massachusetts
BRUCE FISCHL
Affiliation:
MGH-NMR Center, Massachusetts General Hospital, Harvard University, Cambridge, Massachusetts
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Abstract

The aim of the study was to investigate whether age affects visual memory retention across extended time intervals. In addition, we wanted to study how memory capabilities across different time intervals are related to the volume of different neuroanatomical structures (right hippocampus, right cortex, right white matter). One test of recognition (CVMT) and one test of recall (Rey-Osterrieth Complex Figure Test) were administered, giving measures of immediate recognition/recall, 20–30 min recognition/recall, and recognition/recall at a mean of 75 days. Volumetric measures of right hemisphere hippocampus, cortex, and white matter were obtained through an automated labelling procedure of MRI recordings. Results did not demonstrate a steeper rate of forgetting for older participants when the retention intervals were increased, indicating that older people have spared ability to retain information in the long-term store. Differences in neuroanatomical volumes could explain up to 36% of the variance in memory performance, but were not significantly related to rates of forgetting. Cortical volume and hippocampal volume were in some cases independent as predictors of memory function. Generally, cortical volume was a better predictor of recognition memory than hippocampal volume, while the 2 structures did not differ in their predictive power of recall abilities. While neuroanatomical volumetric differences can explain some of the differences in memory functioning between younger and older persons, the hippocampus does not seem to be unique in this respect. (JINS, 2005, 11, 2–15.)

Keywords

Visual memoryHippocampusCortexMRI
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 11 , Issue 1 , January 2005 , pp. 2 - 15
Copyright
© 2005 The International Neuropsychological Society

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References

REFERENCES

Albert, M.S. & Moss, M.B. (1988). Geriatric neuropsychology. New York: Guilford Press.
Alvarez, P., Zola-Morgan, S., & Squire, L.R. (1995). Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. Journal of Neuroscience, 15, 3796–3807.Google Scholar
Anderson, N.D., Craik, F.I.M., & Naveh-Benjamin, M. (1998). The attentional demands of encoding and retrieval in younger and older adults: 1. Evidence from divided attention costs. Psychology and Aging, 13, 405–425.Google Scholar
Barber, R., McKeith, I.G., Ballard, C., Gholkar, A., & O'Brien, J.T. (2001). A comparison of medial and lateral temporal lobe atrophy in dementia with Lewy bodies and Alzheimer's disease: Magnetic resonance imaging volumetric study. Dementia and Geriatric Cognitive Disorders, 12, 198–205.Google Scholar
Beck, A.T. (1987). Beck Depression Inventory. San Antonio, TX: The Psychological Corporation.
Brown, M.W. & Aggleton, J.P. (2001). Recognition memory: What are the roles of perirhinal cortex and hippocampus? Nature Reviews Neuroscience, 2, 51–61.Google Scholar
Brown, J.W. & Jaffe, J. (1975). Hypothesis on cerebral dominance. Neuropsychologia, 13, 107–110.Google Scholar
Buzsaki, G. (1996). The hippocampal-neocortical dialogue. Cerebral Cortex, 6, 81–92.CrossRefGoogle Scholar
Cabeza, R. (2002). Hemispheric asymmetry reduction in old adults: The HAROLD Model. Psychology of Aging, 17, 85–100.Google Scholar
Cahn, D.A., Sullivan, E.V., Shear, P.K., Marsh, L., Fama, R., Lim, K.O., Yesavage, J.A., Tinklenberg, J.R., & Pfefferbaum, A. (1998). Structural MRI correlates of recognition memory in Alzheimer's disease. Journal of the International Neuropsychological Society, 4, 106–114.CrossRefGoogle Scholar
Chantôme, M., Perruchet, P., Hasboun, D., Dormont, D., Sahel, M., Sourour, N., Zouaoui, A., Marsault, C., & Duyme, M. (1999). Is there a negative correlation between explicit memory and hippocampal volume? NeuroImage, 10, 589–595.Google Scholar
Courchesne, E., Chisum, H.J., Townsend, J., Cowles, A., Covington, J., Egaas, B., Harwood, M., Hinds, S., & Press, G.A. (2000). Normal brain development and aging: Quantitative analysis at in vivo MR imaging in healthy volunteers. Neuroradiology, 216, 672–682.Google Scholar
Cullum, C.M., Butters, N., Tröster, A.I., & Salmon, D.P. (1990). Normal aging and forgetting rates on the Wechsler Memory Scale–Revised. Archives of Clinical Neuropsychology, 5, 23–30.CrossRefGoogle Scholar
Daselaar, S.M., Veltman, D.J., Rombouts, S.A.R.B., Raaijmakers, J.G., & Jonker, C. (2003). Deep processing activates the medial temporal lobe in young but not in old adults. Neurobiology of Aging, 24, 1005–1011.CrossRefGoogle Scholar
Delaney, R.C., Prevey, M.L., Cramer, L., & Mattson, R.H. (1988). Test-retest comparability and control subject data for the PASAT, Rey-AVLT, and Rey-Osterreith/Taylor figures [Abstract]. Journal of Clinical and Experimental Neuropsychology, 10, 44.Google Scholar
DeLeon, M.J., Convit, A., George, A.E., Golomb, J., de Santi, S., Tarshish, C., Rusinek, H., Bobinski, M., Ince, C., Miller, D., & Wisniewski, H.M.. (1996). In vivo structural studies of the hippocampus in normal aging and in incipient Alzheimer's disease. Annals of the New York Academy of Sciences, 777, 1–13.Google Scholar
DeLeon, M.J., George, A.E., Golomb, J., Tarshish, C., Convit, A., Kluger, A., de-Santi, S., McCrae, T., Ferris, S.H., Reisberg, B., Ince, C., Rusinek, H., Bobinski, M., Quinn, B., Miller, D.C., & Wisniewkski, H.M. (1997). Frequency of hippocampal formation atrophy in normal aging and Alzheimer's disease. Neurobiology of Aging, 18, 1–11.Google Scholar
de Toledo-Morrell, L., Dickerson, B., Sullivan, M.P., Spanovic, C., Wilson, R., & Bennett, D.A. (2000). Hemispheric differences in hippocampal volume predict verbal and spatial memory performance in patients with Alzheimer's disease. Hippocampus, 10, 136–142.Google Scholar
Deweer, B., Lehericy, S., Pillon, B., Baulac, M., Chiras, J., Marsault, C., Agid, Y., & Dubois, B. (1995). Memory performanve in probable Alzheimer's disease: The role of hippocampal atrophy as shown with MRI. Journal of Neurology, Neurosurgery and Psychiatry, 58, 590–597.CrossRefGoogle Scholar
Dolcos, F., Rice, H.J., & Cabeza, R. (2002). Hemispheric asymmetry and aging: Right hemisphere decline or asymmetry reduction. Neuroscience and Biobehavioral Reviews, 26, 819–825.Google Scholar
Dupont, S., Samson, Y., Le Bihan, D., & Baulac, M. (2002). Anatomy of verbal memory: A functional MRI study. Surgical and Radiologic Anatomy, 24, 57–63.Google Scholar
Eldridge, L.L., Knowlton, B.J., Furmanski, C.S., Bookheimer, S.Y., & Engel, S.A. (2000). Remembering episodes: The selective role of hippocampus in episodic memory. Nature Neuroscience, 3, 1149–1152.Google Scholar
Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., van der Kouwe, A., Killiany, R., Kennedy, D., Klaveness, S., Montillo, A., Makris, N., Rosen, B., & Dale, A.M. (2002). Whole brain segmentation. Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341–355.Google Scholar
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state.” Journal of Psychiatric Research, 12, 189–198.Google Scholar
Fox, N.C., Warrington, E.K., Freeborough, P.A., Hartikainen, P., Kennedy, A.M., Stevens, J.M., & Rossor, M.N. (1996). Presymptomatic hippocampal atrophy in Alzheimer's disease: A longitudinal MRI study. Brain, 119, 2001–2007.Google Scholar
Geffen, G., Moar, K.J., O'Hanlon, A.P., Clark, C.R., & Geffen, L.B. (1990). Performance measures of 16- to 86-year old males and females on the Auditory Verbal Learning Test. Clinical Neuropsychologist, 4, 45–63.Google Scholar
Golomb, J., Kruger, A., De Leon, M.J., Ferris, S.H., Mittelman, M., Cohen, J., & George, A.E. (1994). Hippocampal formation size in normal human aging: A correlate of delayed secondary memory performance. Learning and Memory, 1, 45–54.Google Scholar
Hackert, V.H., den Heijer, T., Oudkerk, M., Koudstaal, P.J., Hofman, A., & Breteler, M.M. (2002). Hippocampal head size associated with verbal memory performance in nondemented elderly. NeuroImage, 17, 1365–1372.Google Scholar
Haist, F., Gore, J.B., & Mao, H. (2001). Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nature Neuroscience, 4, 1139–1145.CrossRefGoogle Scholar
Heun, R., Mazanek, M., Atzor, K.R., Tintera, J., Gawehn, J., Burkart, M., Gaensicke, M., Falkai, P., & Stoeter, P. (1997). Amygdala hippocampal atrophy and memory performance in dementia of Alzheimer type. Dementia and Geriatric Cognitive Disorders, 8, 329–336.CrossRefGoogle Scholar
Huppert, F.A. & Piercy, M. (1979). Normal and abnormal forgetting in inorganic amnesia. Effect of locus of lesion. Cortex, 15, 385–390.Google Scholar
Huppert, F.A. & Kopelman, M.D. (1989). Rates of forgetting in normal aging: A comparison with dementia. Neuropsychologia, 27, 385–390.Google Scholar
Jack, C.R., Petersen, R.C., Xu, Y.C., O'Brien, P.C., Smith, G.E., Ivnik, R.J., Tangalos, E.G., & Kokmen, E. (1997). Rate of medial temporal atrophy in typical aging and Alzheimer's disease. Neurology, 51, 993–999.Google Scholar
Jernigan, T.L., Archibald, S.L., Fennema-Notestine, C., Gamst, A.C., Stout, J.C., Bonner, J., & Hesselink, J.R. (2001). Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiology of Aging, 22, 581–594.Google Scholar
Kelley, W.M., Miezin, F.M., McDermott, K.B., Buckner, R.L., Raichle, M.E., Cohen, N.J., Ollinger, J.M., Akbudak, E., Conturo, T.E., Snyder, A.Z., & Petersen, S.E. (1998). Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron, 20, 927–936.Google Scholar
Kuzniecky, R.I. & Jackson, G.D. (1995). Magnetic resonance in epilepsy. New York: Raven Press.
Köhler, S., Black, S.E., Sinden, M., Szekely, C., Kidron, D., Parker, J.L., Foster, J.K., Moscovitch, M., Winocour, G., Szalai, J.P., & Bronskill, M.J. (1998). Memory impairments associated with hippocampal versus para-hippocampal-gyrus atrophy: An MR volumetry study in Alzheimer's disease. Neuropsychologia, 36, 901–914.Google Scholar
Lezak, M.D. (1995). Neuropsychological assessment (3rd ed.). Oxford, UK: Oxford University Press.
Martin, A., Wiggs, C.L., & Weisberg, J. (1997). Modulation of human medial temporal lobe activity by form, meaning, and experience. Hippocampus, 7, 587–593.3.0.CO;2-C>CrossRefGoogle Scholar
Martone, M., Butters, N., & Traumer, D. (1986). Some analyses of forgetting of pictorial material in amnesic and demented patients. Journal of Clinical and Experimental Neuropsychology, 8, 161–178.CrossRefGoogle Scholar
Mega, M.S., Small, G.W., Xu, M.L., Felix, J., Manese, M., Tran, N.P., Dailey, J.I., Ercoli, L.M., Bookheimer, S.Y., & Toga, A.W. (2002). Hippocampal atrophy in persons with age-associated memory impairment: Volumetry within a common space. Psychosomatic Medicine, 64, 487–492.CrossRefGoogle Scholar
Milner, B. (1968). Visual recognition and recall after right temporal-lobe excision in man. Neuropsychologia, 6, 191–209.Google Scholar
Milner, B. (1972). Disorders of learning and memory after temporal lobe lesions in man. Clinical Neurosurgery, 19, 421–446.Google Scholar
Monk, C.S., Zhuang, J., Curtis, W.J., Ofenloch, I.-T., Tottenham, N., Nelson, C.A., & Hu, X. (2002). Human hippocampal activation in the delayed matching- and nonmatching-to-sample memory tasks: An event-related functional MRI approach. Behavioral Neuroscience, 116, 716–721.Google Scholar
Mori, E., Yoneda, Y., Yamashita, H., Hirono, N., Ikeda, M., & Yamadori, A. (1997). Medial temporal structures related to memory impairment in Alzheimer's disease: An MRI volumetric study. Journal of Neurology, Neurosurgery and Psychiatry, 63, 214–221.Google Scholar
O'Brien, J.T., Desmond, P., Ames, D., Schweitzer, I., Chiu, E., & Tress, B. (1997). Temporal lobe magnetic resonance imaging can differentiate Alzheimer's disease from normal aging, depression, vascular dementia and other causes of cognitive impairment. Psychological Medicine, 27, 1267–1275.Google Scholar
Osterrieth, P.A. (1993). Complex Figure Copy Test. J. Corwin & F.W. Bylsma, Trans. The Clinical Neuropsychologist, 7, 9–15. Reprinted from Osterrieth, P.A. (1944). Le test de copie d'une figure complexe. Archives de Psychologie, 30, 206–356.Google Scholar
Pakkenberg, B. & Gundersen, H.J.G. (1997). Neocortical neuron number in humans: Effect of sex and age. Journal of Comparative Neurology, 384, 312–320.3.0.CO;2-K>CrossRefGoogle Scholar
Parkin, A.J. (1993). Memory. Phenomena, experiment and theory. Oxford, UK: Blackwell.
Peters, A., Morrison, J., Rosene, D., & Hyman, B. (1998). Are neurons lost from the primate cerebral cortex during normal aging? Cerebral Cortex, 8, 295–300.Google Scholar
Petersen, R.C., Jack, C.R., Xu, Y.C., Waring, S.C., O'Brien, P.C., Smith, G.E., Ivnik, R.J., Tangalos, E.G., Boeve, B.F., & Kokmen, E. (2000). Memory and MRI-based hippocampal volumes in aging and AD. Neurology, 54, 581–592.Google Scholar
Rapp, P.R., Deroche, P.S., Mao, Y., & Burwell, R.D. (2002). Neuron number in the parahippocampal region is preserved in aged rats with spatial learning deficits. Cerebral Cortex, 12, 1171–1179.Google Scholar
Raz, N., Gunning, F.M., Head, D., Dupuis, J.H., McQuain, J., Briggs, S.D., Loken, W.J., Thornton, A.E., & Acker, J.D. (1997). Selective aging of the human cerebral cortex observed in vivo: Differential vulnerability of the prefrontal grey matter. Cerebral Cortex, 7, 268–282.CrossRefGoogle Scholar
Raz, N., Gunning-Dixon, F.M., Head, D., Dupuis, J.H., & Acker, J.D. (1998). Neuroanatomical correlates of cognitive aging: Evidence from structural magnetic resonance imaging. Neuropsychology, 12, 95–114.Google Scholar
Regeur, L., Badsberg Jensen, G., Pakkenberg, H., Evans, S.M., & Pakkenberg, B. (1994). No global neocortical nerve cell loss in brains from patients with senile dementia of Alzheimer's type. Neurobiology of Aging, 15, 347–352.Google Scholar
Rempel-Clower, N.L., Zola, S.M., Squire, L.R., & Amaral, D.G. (1996). Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. Journal of Neuroscience, 16, 5233–5255.Google Scholar
Rey, A. (1993). Psychological examination of traumatic encephalopathy. (J. Corwin & F.W. Bylsma, Trans.) The Clinical Neuropsychologist, 1, 4–9. (Reprinted from Rey, A. (1941). Archives de Psychologie, 28, 286–340).Google Scholar
Riedel, G. & Micheau, J. (2001). Function of the hippocampus in memory formation: Desperately seeking resolution. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 25, 835–853.Google Scholar
Rosselli, M. & Ardila, A. (1991). Effects of age, education and gender on the Rey-Osterrieth Complex Figure. Clinical Neuropsychologist, 5, 370–376.CrossRefGoogle Scholar
Rybarczyk, B.D., Hart, R.P., & Harkins, S.W. (1987). Age and forgetting rate with pictorial stimuli. Psychology and Aging, 2, 404–406.Google Scholar
Schuff, N., Amend, D.L., Knowlton, R., Norman, D., Fein, G., & Weiner, M.W. (1999). Age-related metabolite changes and volume loss in the hippocampus by magnetic resonance spectroscopy and imaging. Neurobiology of Aging, 20, 279–285.Google Scholar
Scoville, W.B. & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry, 20, 11–21.Google Scholar
Simic, G., Kostovic, I., Winblad, B., & Bogdanovic, N. (1997). Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. Journal of Comparative Neurology, 379, 482–494.3.0.CO;2-Z>CrossRefGoogle Scholar
Small, S.A., Perera, G.M., DeLaPaz, R., Mayeux, R., & Stern, Y. (1999). Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer's disease. Annals of Neurology, 45, 466–472.3.0.CO;2-Q>CrossRefGoogle Scholar
Small, S.A., Stern, Y., Tang, M., & Mayeux, R. (1999). Selective decline in memory function among healthy elderly. Neurology, 52, 1392–1396.CrossRefGoogle Scholar
Small, S.A., Tsai, W.Y., & DeLaPaz, R. (2002). Imaging hippocampal function across the human life span: Is memory decline normal or not? Annals of Neurology, 51, 290–295.Google Scholar
Spikman, J.M., Berg, I.J., & Deelman, B.G. (1995). Spared recognition capacity in elderly and closed-head injury subjects with clinical memory deficits. Journal of Clinical and Experimental Neuropsychology, 17, 29–34.Google Scholar
Spreen, O. & Strauss, E. (1991). A compendium of neuropsychological tests: Administration, norms, and commentary. New York: Oxford University Press.
Stebbins, G.T., Carrillo, M.C., Dorfman, J., Dirksen, C., Desmond, J.E., Turner, D.A., Bennett, D.A., Wilson, R.S., Glover, G., & Gabrieli, J.D. (2002). Aging effects on memory encoding in the frontal lobes. Psychology and Aging, 17, 44–55.CrossRefGoogle Scholar
Taylor, M.L. (1979). Psychological assessment of neurosurgical patients. In T. Rasmussen & R. Marino (Eds.), Functional neurosurgery (pp. 165–180). New York: Raven Press.
Terry, R.D., Deteresa, R., & Hansen, L.A. (1987). Neocortical cell counts in normal human adult aging. Annals of Neurology, 21, 530–539.CrossRefGoogle Scholar
Tisserand, D.J., Visser, P.J., van Boxtel, M.P.J., & Jolles, J. (2000). The relation between global and limbic brain volumes on MRI and cognitive performance in healthy individuals across the age range. Neurobiology of Aging, 21, 569–576.Google Scholar
Tombaugh, T.N. & Hubley, A.M. (2001). Rates of forgetting on three measures of verbal learning using retention intervals ranging from 20 min to 62 days. Journal of the International Neuropsychological Society, 7, 79–91.CrossRefGoogle Scholar
Trahan, D.E. (1985). Analysis of gender differences in verbal and visual memory [Abstract]. Journal of Clinical and Experimental Neuropsychology, 7, 640–641.Google Scholar
Trahan, D.E. & Larrabee, G.J. (1985). Visual recognition memory is patients with closed head trauma, Alzheimer's type dementia, and amnestic syndrome [Abstract]. Journal of Clinical and Experimental Neuropsychology, 7, 640.Google Scholar
Trahan, D.E. & Larrabee, G.J. (1988). Continuous Visual Memory Test. Odessa, FL: Psychological Assessment Resources.
Trahan, D.E. & Larrabee, G.J. (1992). Effects of normal aging on rate of forgetting. Neuropsychology, 6, 115–122.CrossRefGoogle Scholar
Trahan, D.E., Larrabee, G.J., & Quintana, J.W. (1990). Visual recognition memory in normal adults and patients with unilateral vascular lesions. Journal of Clinical and Experimental Neuropsychology, 12, 857–872.Google Scholar
Ungerleider, L.G. (1995). Functional brain imaging studies of cortical mechanisms for memory. Science, 270, 769–775.CrossRefGoogle Scholar
Walhovd, K.B., Fjell, A.M., Reinvang, I., Lundervold, A., Fischl, B., Quinn, B.T., & Dale, A.M. (2004). Size does matter in the long run—Hippocampal and cortical volume predict recall across weeks. Neurology, 63, 1193–1197.CrossRefGoogle Scholar
Walhovd, K.B. & Fjell, A.M. (2003). The relationship between P3 and neuropsychological function in an adult life span sample. Biological Psychology, 62, 65–87.CrossRefGoogle Scholar
Ward, M.T., Oler, J.A., & Markus, E.J. (1999). Hippocampal dysfunction during aging I: Deficits in memory consolidation. Neurobiology of Aging, 20, 363–372.Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: The Psychological Corporation.
Wickelgren, W. (1975). Age and storage dynamic in continuous recognition memory. Developmental Psychology, 11, 165–169.CrossRefGoogle Scholar
Wicket, J.C., Vernon, P.A., & Lee, D.H. (2000). Relationships between factors of intelligence and brain volume. Personality and Individual Differences, 29, 1095–1122.Google Scholar
Ylikoski, R., Salonen, O., Mäntylä, R., Ylikoski, A., Keskivaara, P., Leskelä, M., & Erkinjuntti, T. (2000). Hippocampal and temporal lobe athrophy and age-related decline in memory. Acta Neurologica Scandinavica, 101, 273–278.Google Scholar
Youngjohn, J.R. & Crook, T.H. (1993). Learning, forgetting and retrieval of everyday material across the adult lifespan. Journal of Clinical and Experimental Neuropsychology, 15, 447–460.Google Scholar
Zola-Morgan, S. & Squire, L.R. (1996). Neuroanatomy of memory. Annual Review of Neuroscience, 16, 547–563.Google Scholar
Zola, S.M., Squire, L.R., Teng, E., & Stefanacci, L. (2000). Impaired recognition memory in monkeys after damage limited to the hippocampal region. Journal of Neuroscience, 20, 451–463.Google Scholar