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Medial Temporal Structures Relate to Memory Impairment in Alzheimer's

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Medial Temporal Structures Relate to Memory Impairment in Alzheimer's J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.63.2.214 on 1 August 1997. Downloaded from 214 Journal of Neurology, Neurosurgery, and Psychiatry 1997;63:214–221 Medial temporal structures relate to memory impairment in Alzheimer’s disease: an MRI volumetric study Etsuro Mori, Yukihiro Yoneda, Hikari Yamashita, Nobutsugu Hirono, Manabu Ikeda, Atsushi Yamadori Abstract predominantly aVect regions of the limbic and Objectives—Memory impairment is not paralimbic medial temporal structures and only the earliest clinical symptom but a association areas of the neocortex.1–3 There is a central and prominent feature throughout significant correlation between severity of the course of Alzheimer’s disease. Alz- dementia in Alzheimer’s disease and these heimer related pathological alterations in postmortem neuropathological findings.4–6 The the medial temporal structures may ac- neuropathological changes in the medial tem- count for the memory impairments in poral lobe may account for memory impair- patients with Alzheimer’s disease. The ment in Alzheimer’s disease7; this is not only aim of this study was to elucidate the role the earliest clinical symptom but a central and of the medial temporal structures in prominent feature throughout the course of the memory impairment caused by Alzheim- disease. In vivo neuroimaging techniques have er’s disease. shown a relation between memory impairment Methods—Using high resolution MRI and and the degree of medial temporal damage a semiautomated image analysis tech- expressed as atrophy on MRI and hypoper- nique, volumes of the medial temporal fusion or hypometabolism shown by PET.8 The structures (amygdaloid complex, hippo- hippocampus is a central component of the campal formation, subiculum, and para- medial temporal lobe memory system, and its hippocampal gyrus) were measured, and structural integrity is necessary for declarative correlations between atrophy of each memory.9 The cortex adjacent to the hippoc- structure and memory dysfunction in ampus, including entorhinal, perirhinal, and patients with Alzheimer’s disease were parahippocampal cortices, is not simply a con- examined. duit for connecting the neocortex to the Results—Patients with Alzheimer’s dis- hippocampus, but is actively involved in ease showed poor performance on verbal storage of information from the neocortex and non-verbal memory tests, and MRI before reaching the hippocampus itself.9 De- volumetry showed a significant volume struction restricted to the bilateral hippocampi Department of Clinical reduction of the medial temporal lobe Neurosciences, Hyogo is known to produce memory deficits in http://jnnp.bmj.com/ Institute for Aging structures. Volumes of the amygdaloid animals10 and in humans.11 There is neuroim- Brain and Cognitive complex and of the subiculum correlated aging evidence for loss of hippocampal tissue in Disorders with memory performance. Stepwise human diseases associated with memory E Mori regression analyses disclosed that the vol- 12 13 H Yamashita impairments. Furthermore, the perirhinal ume of the right amygdaloid complex spe- cortex and the closely associated parahippoc- N Hirono cifically predicted visual memory M Ikeda ampal cortex provide the major source of cor- function and to some extent verbal tical input to the hippocampal formation,9 and Neurology Service, memory function, and that the volume of CA1 pyramidal cells send eVerent fibres to the on September 25, 2021 by guest. Protected copyright. Hyogo Brain and the left subiculum specifically predicted subiculum, entorhinal cortex, and several sub- Heart Center at verbal memory function. Atrophy of the cortical areas.14 Bilateral lesions limited to Himeji hippocampus did not predict severity of these areas produce severe memory impair- Y Yoneda memory impairment. ment in monkeys.15 16 Although the amygdala is —The presence of perihip- Section of Conclusions not a part of the medial temporal lobe memory pocampal damage involving the amygdala Neuropsychology, system for the processing of declarative proper, its surrounding cortex, and the Division of Disability memory,9 there is evidence indicating that Science, Tohoku subiculum further increased the severity lesions in the amygdala produce memory defi- University Graduate of memory impairment attributable to cits in humans and animals.17–21 However, there School of Medicine hippocampal damage in Alzheimer’s dis- A Yamadori is a controversy over whether damage to the ease. amygdala contributes to the severity of Correspondence to: memory loss. Recent studies have indicated Dr Etsuro Mori, Clinical (J Neurol Neurosurg Psychiatry 1997;63:214–221) Neurosciences, Hyogo that the additive eVect of damage to the Institute for Aging Brain and Keywords: Alzheimer’s disease; magnetic resonance amygdala on hippocampal damage is not a Cognitive Disorders, 520 consequence of damage to the amygdala itself Saisho-ko, Himeji, 670, imaging; memory; medial temporal lobe Japan. but is due to involvement of the adjacent corti- ces (periamygdala, entorhinal, and perirhinal Received 3 September 1996 Neuropathological changes in Alzheimer’s dis- cortices) covering the surface of the amygdala and in final revised form 9152223 13 January 1997 ease include neurofibrillary tangles, senile and parahippocampal gyrus. The role of Accepted 6 March 1997 plaques, and neuronal and synaptic loss and the amygdaloid complex, hippocampus, J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.63.2.214 on 1 August 1997. Downloaded from Memory impairment in Alzheimer’s disease 215 subiculum, and parahippocampal gyrus in for Aging Brain and Cognitive Disorders, memory impairment in patients with Alzheim- Himeji Japan, and was approved by the internal er’s disease remains unestablished. review board in 1993. After a complete Medial temporal atrophy is present on CT description of the study to the subjects and and MRI in most patients with Alzheimer’s their relatives, written consent was obtained. disease, and in vivo direct measurement of brain volume with MRI has emerged as the best method to quantify it.24–31 Volumetric MRI VOLUMETRY studies have examined the relation between Brain MRI was performed on a 1.5 T MRI medial temporal lobe atrophy and memory scanner (Signa Advantage 5x, General Elec- impairments in diseases and aging.13 24–36 In the tric) with the use of a circularly polarised head present study, to elucidate the structural deter- coil as both transmitter and receiver. Coronal minants of severity of impairment of memory 3D spoiled gradient echo (SPGR) images (field × × within the medial temporal structures in of view of 220 mm, matrix of 256 256, 124 patients with Alzheimer’s disease, we directly 1.5 mm contiguous sections, TR 14 ms, TE 3 ° measured the volume of these structures (amy- ms, flip angle 20 ) perpendicular to the gdaloid complex, hippocampal formation, anterior-posterior commissure plane covering subiculum, and parahippocampal cortex) using the whole calvarium were used for the 41 semiautomated image processing of high reso- volumetric study. Axial T2 weighted proton lution MRI, and analysed the relation between density, and T1 weighted images were also atrophy of each structure and memory dys- obtained for diagnosis. function. The MRI data sets of all images were directly transmitted to a personal computer (Power Macintosh 8100/80, Apple) and analysed using Methods the public domain NIH Image version 1.59 SUBJECTS program (written by Wayne Rasband at the US Forty six Japanese patients with mild to National Institutes of Health and available moderate Alzheimer’s disease were selected from the internet by anonymous ftp from among those admitted to our hospital for zippy.nimh.nih.gov or on floppy disk from investigation between July 1993 and March NTIS, 5285 Port Royal Rd, Springfield, VA 1995. All patients were examined by neurolo- 22161, part number PB93–504868) with resi- gists and psychiatrists. Routine laboratory dential macroprograms developed in our insti- tests, standard neuropsychological examina- tute after an appropriate data conversion. tions, EEG, MRI of the brain, magnetic All volume measurements were performed resonance angiography of the neck and head, by a segmentation technique with a combina- and cerebral perfusion and metabolism studies tion of tracing and thresholding. The volume of by PET or single photon emission computed a given structure in each slice was obtained by tomography (SPECT) were performed in all automatically counting the number of pixels patients. The inclusion criteria comprised (1) a within the segmented regions and multiplying diagnosis of probable Alzheimer’s disease the number by a voxel size (220/2562 × 1.5 = according to the NINCDS/ADRDA criteria,37 1.108 mm3). One investigator (YY) measured (2) age younger than 80 years, and (3) mild to the volume of the medial temporal structures http://jnnp.bmj.com/ moderate functional impairment (grades 0.5, and one (EM) the intracranial volumes. We 1, and 2 on the clinical dementia scale38). used a semiautomatic segmentation technique Patients were excluded if; (1) other through density thresholding, thereby avoiding neurological or systemic diseases were present, the partial voluming and observer’s bias. The (2) a mini mental state examination test-retest reliability, measured using an intrac- (MMSE)39 40 score less than 11 suggested the lass correlation coeYcient derived from three presence of severe language, attention, and repeated measurements by one rater under behavioural disorders that would make the
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