Volumetric MRI analysis of the amygdala and the hippocampus in subjects with age‐associated memory impairment

Age-associated memory impairment (AAMI) is a common but disputed entity. It is unclear whether AAMI is a phenomenon of normal aging or an early sign of Alzheimer's disease. The present study aimed to identify possible structural abnormalities in the medial temporal lobe of AAMI subjects. We measured volumes of the hippocampus and amygdala by MRI in 16 AAMI subjects and in 16 age- and sex-matched controls and correlated the volumes with subjects' performance on two visual memory tasks (the Benton and the Heaton visual retention tests) and on a verbal memory task (the Buschke-Fuld Selective Reminding Test). The mean hippocampal and amygdaloid volumes normalized for brain size per se did not differ between the two study groups. In controls, but not in AAMI subjects, the right hippocampus was larger than the left. Accordingly, the volumetric asymmetry between the right and left hippocampi was smaller in AAMI subjects than in controls (Student's t test, p <0.05). The volume of the right hippocampus (r = 0.37, n = 32, p <0.05) and the magnitude of the asymmetry between the right and left hippocampi (r = 0.38, n = 32, p <0.05) correlated with total score on the Benton test. We also found significant correlations between the amygdaloid volumes and the performance on visual memory tests but not with score on the verbal memory test. Furthermore, a subgroup of seven AAMI subjects with the lowest visual memory scores (≤5 on the Benton test) had smaller right and left amygdala (13%, p <0.05) than the six controls with the highest scores (=9 on the Benton test). Thus, we demonstrate that minor structural changes are present in both the hippocampus and the amygdala in AAMI subjects compared with age-matched controls. Follow-up of the subjects will be necessary to determine whether these minor structural abnormalities predict development of dementia or just reflect increased variability of cognitive performance in elderly humans.

[1]  E. Tangalos,et al.  Memory function in normal aging , 1992, Neurology.

[2]  G. Murphy,et al.  Volumetric asymmetry in the human amygdaloid complex. , 1987, Journal fur Hirnforschung.

[3]  L. Squire,et al.  Memory impairment in monkeys following lesions limited to the hippocampus. , 1986, Behavioral neuroscience.

[4]  L. Squire,et al.  Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  R. Pearson,et al.  The Human Nervous System. Basic Elements of Structure and Function , 1967, The Yale Journal of Biology and Medicine.

[6]  M. Mishkin,et al.  The neuroanatomy of amnesia: amygdala-hippocampus versus temporal stem. , 1982, Science.

[7]  T. Crook,et al.  Age-associated memory impairment: diagnostic criteria and treatment strategies. , 1988, Psychopharmacology bulletin.

[8]  M. Laakso,et al.  Population-Based Dementia Screening Program in Kuopio: The Effect of Education, Age, and Sex on Brief Neuropsychological Tests , 1992, Journal of geriatric psychiatry and neurology.

[9]  E. Tangalos,et al.  Age-associated memory impairment diagnoses: problems of reliability and concerns for terminology. , 1991, Psychology and aging.

[10]  A. Benton,et al.  The visual retention test as a constructional praxis task. , 1962, Confinia neurologica.

[11]  D R Fish,et al.  Hippocampal volumetric and morphometric studies in frontal and temporal lobe epilepsy. , 1992, Brain : a journal of neurology.

[12]  D. Munoz,et al.  Hippocampal sclerosis and human memory. , 1993, Archives of neurology.

[13]  David G. Amaral,et al.  Individual differences in the cognitive and neurobiological consequences of normal aging , 1992, Trends in Neurosciences.

[14]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  S. Ferris,et al.  Age‐associated memory impairment: Proposed diagnostic criteria and measures of clinical change — report of a national institute of mental health work group , 1986 .

[16]  M. Mishkin,et al.  Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  Stephen W. Scheff,et al.  Volumetric atrophy of the amygdala in Alzheimer's disease , 1991, Neurology.

[18]  M Ashtari,et al.  Three-dimensional fast low-angle shot imaging and computerized volume measurement of the hippocampus in patients with chronic epilepsy of the temporal lobe. , 1991, AJNR. American journal of neuroradiology.

[19]  B T Hyman,et al.  Neuropsychological correlates of bilateral amygdala damage. , 1990, Archives of neurology.

[20]  F Andermann,et al.  Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging , 1992, Neurology.

[21]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[22]  F. Craik,et al.  Changes in memory with normal aging: a functional view. , 1990, Advances in neurology.

[23]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[24]  G A Press,et al.  Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  C. Jack,et al.  Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. , 1989, Radiology.

[26]  C. Coffey,et al.  Quantitative cerebral anatomy of the aging human brain , 1992, Neurology.

[27]  O Nalcioglu,et al.  Quantification of magnetic resonance scans for hippocampal and parahippocampal atrophy in Alzheimer's disease , 1991, Neurology.

[28]  B. Reisberg,et al.  Longitudinal course of normal aging and progressive dementia of the Alzheimer's type: A prospective study of 106 subjects over a 3.6 year mean interval , 1986, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[29]  Alan C. Evans,et al.  MRI of Amygdala and Hippocampus in Temporal Lobe Epilepsy , 1993, Journal of computer assisted tomography.

[30]  L. Goldstein The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1992, The Yale Journal of Biology and Medicine.

[31]  D. Wechsler A Standardized Memory Scale for Clinical Use , 1945 .

[32]  The Human Hippocampus , 1989, Neurology.

[33]  HERMAN BUSCHKE,et al.  Evaluating storage, retention, and retrieval in disordered memory and learning , 1974, Neurology.

[34]  W. Jagust,et al.  Quantitative NMR measurements of hippocampal atrophy in Alzheimer's disease , 1988, Magnetic resonance in medicine.

[35]  C R Jack,et al.  Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. , 1990, Radiology.

[36]  C R Jack,et al.  Magnetic resonance imaging–based volume studies in temporal lobe epilepsy: Pathological correlations , 1991, Annals of neurology.

[37]  M. Mishkin Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus , 1978, Nature.

[38]  C R Jack,et al.  Temporal Lobe Volume Measurement from MR Images: Accuracy and Left‐Right Asymmetry in Normal Persons , 1988, Journal of computer assisted tomography.

[39]  E. Caine,et al.  Does "benign senescent forgetfulness" exist? , 1988, Clinics in geriatric medicine.