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Introduction Journal ofVestibularResearcn, VoL 1, 1~u. L, PP·,, ~~, -- _ Copyright © 1997 Elsevier Science Inc. Printed in the USA. All rights reserved 0957-4271/97 $17.00 + .00 Pll 80957-4271(96)00137-1 Original Contribution AGING AND THE HUMAN VESTIBULAR NUCLEUS Ivan Lopez,* Vicente Honrubia,* and Robert W. Baloh,*t UCLA School of Medicine, *Division of Head and Neck Surgery, tDepartment of Neurology, Los Angeles, California Reprint address: Robert W. Baloh, M.D., Department of Neurology, UCLA School of Medicine, Los Angeles, CA 90024-1769; Tel: (310) 825-5910; Fax: (310) 206-1513 0 Abstract-Degenerative changes during aging Introduction have been identified in the inner ear and in the vestibular nerve, but not in the human vestibular Complaints of dizziness and disequilibrium are nuclear complex (VNC). Therefore, the purpose of extremely common in older people (1). Associ­ this study was to document quantitative morpho­ ated falls are a major cause of morbidity and mor­ metric changes within the VNC in humans as a function of age. The VN C of normal human sub­ tality (2,3). Age-related morphological changes jects was examined for age-related changes using occur in all of the sensory systems essential for computer-based microscopy. Neuronal counts, nu­ maintaining balance during locomotion. Neu­ clear volume, neuronal density, and nuclear roanatomical studies of the peripheral vestibular length of the 4 vestibular nuclei were determined system have documented a significant loss of in 15 normal people, age 40 to 93 years. Based on a hair cells and primary vestibular neurons as a linear model, there was approximately a 3% neu­ function of age (4,5). Since the vestibular nu­ ronal loss per decade from age forty to ninety. clear complex (VNC) is a major visual-vestibu­ VNC volume and neuronal density also decreased lar interaction center, age-related neuronal loss significantly with age, although to a lesser degree in the VNC could have particularly important than did the number of neurons. Neuronal loss as functional implications. a percentage of the total number of neurons was greatest in the superior vestibular nucleus and There is general agreement that neuronal cell least in the medial vestibular nucleus. Despite the density in the cerebral cortex decreases with overall loss of neurons, the number of giant neu­ age, although the rate of decrease varies with rons (>500 11-m2) increased in older people. This the location (6-8). An age-related loss in the to­ increase in giant neurons could be traced to the tal number of Purkinje cells within the cerebel­ accumulation of lipofuscin deposits in the cell so­ lum is also well documented in humans (9). mata. The overall rate of neuronal loss with aging There is an average of 2.5% Purkinje-cell loss in the VNC is comparable tn that previously ob­ per decade over the age span of 0 to 100 years served in hair cells, primary vestibular neurons, (9). By contrast, quantitative studies of human and cerebellar Purkinje cells, but is in contrast to brain stem nuclei have found relatively little prior reports of no age-related loss of neurons in age-related neuronal loss (7, 10-14). There have other brain stem nuclei. Copyright © 1997 Elsevier been no prior studies of age-related effects on the Science Inc. human VNC, but Sturrock (30) observed a signifi­ cant decrease in the total number of neurons in the lateral vestibular nucleus of the aging mouse. 0 Keywords- quantitative morphometry; aging; The purpose of this study was to document vestibular nucleus. quantitative morphometric changes within the REcEIVED 12 July 1995; AccEPTED 20 August 1996. 77 78 I. Lopez et al VNC in humans as a function of age. These myelin basic protein (MBP). The immunoreac­ measurements will serve as normative data for a tion product was only found in cells less than 40 study on dizziness and disequilibrium in older ~J-m2 . Furthermore, specimens were immunore­ people, sponsored by the National Institutes of acted with antibodies against synaptophysin, Aging. Preliminary results have been reported which stains axodendritic and axosomatic ter­ in abstract form (15). minals. Rarely were cells of less than 40 ~J-m2 surrounded by immunoreactive terminals in young or older subjects. IVIaterials and Methods Although the counting and measuring were done automatically, the operator viewed each Fifteen human brain specimens (7 female, 8 field on a video screen and performed a variety male; ages 40 to 93 years) were obtained within of automatic editing functions. The NIH Image 6 to 24 hours postmortem from subjects who program allows the removal of vascular ele­ had no chronic medical illnesses or known ments and artifacts, separation of contiguous symptoms of nervous system or ear disease cell images, and increased focal detection when prior to death. At postmortem examination, the part of a cell, although visible on the video brains showed no gross evidence of pathology; screen, was not stained with sufficient intensity the cause of death in each case was not neuro­ to be detected automatically for measurement. logicaL The specimens were fixed for 2 weeks Among these functions, "threshold" is used to in 10% buffered formalin, embedded in paraffin, segment an image into objects of interest and and serially sectioned at 20 micrometers. Every background on the basis of gray level. Additional tenth section was stained with a modification of a editing functions like ~'sharpen" and "subtract formaldehyde-thionin technique ( 16). background" are used to increase contrast and ac­ The boundaries of the vestibular nuclei were centuate details of the cells (NIH Image 1.44 outlined according to the criteria of Sadjadpour manual, 1992). This process was done on every and Brodal (Figure 1) (17). The number of neu­ 20th section, that is, 400 1-1m apart. To compute rons in each vestibular nucleus was determined the number of neurons in each 20-section vol­ by using a computer-based video microscopy ume, the estimated number of neurons in each and image analysis system (NIH, 1.44, public analyzed section was multiplied by 20. To domain). An image from each brain stem sec­ avoid multiple counting of cells larger in diame­ tion in the area of the vestibular nucleus was ter than the section thickness, a correction fac­ digitized using a Macintosh II computer tor was used. It was implemented by dividing equipped with a frame grabber attached to a the total number of neurons with a diameter be­ video camera mounted on a photomicroscope. tween 1- and 2-section thickness (that is 20 to The area of each individual vestibular nucleus 40 ~J-ill) by 2, those between 2- and 3-section was manually selected and recorded using the thickness (40 to 60 ~J-ill) by 3, and so on. The cursor. Neurons within this area were identified number of neurons in the vestibular nuclear on the video screen. The number of neurons and complex was determined by adding the number the area of each neuron were automatically de­ of neurons of the 4 vestibular nuclei. termined by the program. The diameter was de­ The volume of each vestibular nucleus was termined by calculating the diameter of a circle computed by multiplying the area of each sec­ of equal area to the neuron using the equation d = tion by the thickness of the section (20 1-1m) and 2 Jareal 1t . Cells with areas greater than or by 10 (periodicity of the analyzed sections). The equal to 40 ~J-m2 were counted as neurons. All volume of the vestibular nuclear complex was cells less than 40 ~J-m2 were considered glia and estimated by adding together the partial volumes excluded from the analysis (19). To confirm of each block. Neuronal density was calculated this assumption, glial cells in brain stem sec­ by dividing the number of neurons by the vol­ tions of both young and older subjects were ume in cubic millimeters. identified by using monoclonal antibodies The length of each individual vestibular nu­ against glial fibrilar acidic protein (GF AP) and cleus was obtained by multiplying the thickness Aging in the Vestibular Nucleus 179 Figure 1. Low-magnification photomicrographs illustrating the location of the four major vestibular nuclei {dot­ ted lines) in the brain stem. (A) superior vestibular nucleus; (B) medial vestibular nucleus; (C) lateral vestibular nucleus; and (D) descending vestibular nucleus. Thionin staining. Bar = 1 mm. of the section by the number of sections that Each vestibular subnucleus also showed a demonstrated the morphometric characteristics significant (p < 0.05) decrease in number of of that nucleus. The length of the VNC was de­ neurons as a function of age. The highest rate of termined by identifying the beginning of the neuronal loss (6% per decade) occurred in the caudal portion of the descending vestibular nu­ superior vestibular nucleus, and the lowest rate cleus and the rostral end of the superior vestibu­ of neuronal loss (3% per decade) occurred in lar nucleus. The number of slides between these the medial vestibular nucleus (Table 1). Vol­ levels was multiplied by the section thickness. ume and neuronal density also decreased with age in each subnucleus, but the decrease was significant (p < 0.05) in only 2 of the 4 nuclei. Results Only the length of the descending nucleus de­ creased significantly (p < 0.05) with age. Regression analysis documented a highly To assess the relationship between neuronal significant (p < 0. 001) decrease with age in the size and age-related neuronal loss, we subdi­ number of neurons in the VNC (Figure 2A). vided neurons into small (40 to 99 1-1m2), me­ The slope of the regression line was similar in dium (100 to 199 f-LITI 2), large (200 to 499 f-LITI2), men and women (r = 0.86 and 0.90, respec­ and giant (>500 f-LITI 2) (Figure 3).
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