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      Life-span dendritic and spine changes in areas 10 and 18 of human cortex: A quantitative golgi study

      , ,
      The Journal of Comparative Neurology
      Wiley

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          Abstract

          Dendritic neuropil is a sensitive indicator of the aging process and may exhibit regional cortical variations. The present study examined regional differences and age-related changes in the basilar dendrites/spines of supragranular pyramidal cells in human prefrontal (area 10) and secondary occipital (area 18) cortices. Tissue was obtained from the left hemisphere of 26 neurologically normal individuals ranging in age from 14 to 106 years (M(age) = 57 +/- 22 years; 13 males, 13 females). In tissue prepared by a modified rapid Golgi technique, ten neurons were sampled from each cortical region (N = 520) and were evaluated according to the following parameters: total dendritic length, mean segment length, dendritic segment count, dendritic spine number, and dendritic spine density. The effects of age and Brodmann areas were analyzed with a nested multiple analysis of variance design. Despite considerable interindividual variation, several clear findings emerged: 1) Dendritic systems were significantly larger in area 10 than in area 18 across the sampled life span, presumably because of the more integrative function of area 10 neurons. 2) There was a significant age effect, with a substantial decline in dendritic neuropil from the younger (< or =50 years) group to the older (>50 years) group, especially in spine measures, which decreased almost 50%. 3) Dendritic values were relatively stable after 40 years of age, suggesting that dendritic/spine degeneration in older, relatively healthy individuals may not be an inevitable consequence of the aging process. These findings underscore the importance of life-long commitment to a cognitively invigorating environment.

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          Most cited references10

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          Genetic variability of human brain size and cortical gyral patterns.

          The development of the primate brain is determined by an interaction of genetic programmes and environmental events. We examined quantitatively the contribution of each of these factors to adult human brain hemisphere volume and global cortical gyral patterns by comparing 3-D MRI renderings of brains of 10 pairs of monozygotic (MZ) and nine pairs of same-sex dizygotic (DZ) twins. Brain volume was highly correlated in MZ pairs [unbiased intraclass correlation coefficient, ICC(U) = 0.95, P < 0.00001], but not in DZ pairs [ICC(U) = 0.35, P = 0.09]. Structural equation modelling indicated a 94% heritability of brain volume. Gyral patterns appeared visually more similar in MZ than in DZ pairs. This was confirmed statistically by a cross-correlation analysis of rendered images of lateral and mesial cortical surfaces. MZ twins exhibited significantly greater similarity than did DZ twins in comparisons of gyral patterns; DZ twins were not more alike than unrelated pairings. Ipsilateral hemispheres were significantly more alike than contralateral hemispheres within MZ pairs, but not within DZ pairs. Contralateral hemispheres within an individual were more alike than contralateral hemispheres between twins in the DZ pairs, but not in the MZ pairs. Heritability for gyral-sulcal patterns, as reflected in the cross-correlation data, was low and ill defined. These results indicate that human cerebral size is determined almost entirely by genetic factors and that overall cortical gyral patterns, though significantly affected by genes, are determined primarily by nongenetic factors.
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            Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: II. Spine distributions.

            The numbers and distributions of dendritic spines were estimated for six adult and three juvenile biocytin-injected neurones from the CA1 region of the hippocampus of the albino rat. For each cell, a sample of long dendritic segments that lay favourably in the plane of focus was drawn at high magnification and the visible spines counted. Correction was made for spines obscured by dendritic shafts. Within individual cells, dendrites of similar type and diameter had similar spine densities. For adults, long basal segments averaged 2.4 spines/microns and obliques averaged 3.2 spines/microns. In juveniles, basals averaged 2.3 spines/microns and obliques, 2.5 spines/microns. Apical tuft segments were less spiny, averaging 1.4 spines/microns in adult cells and 1.8 spines/microns in juveniles. There was a positive correlation between spine density and dendrite diameter. Values from this sample were used to assign spine densities to the other segments, and so the total number of spines was estimated for each cell. Adult cells averaged 30,500 +/- 3,900 (S.D.) spines and juveniles, 23,800 +/- 7,100 spines. Adult cells had roughly 50% of their spines in stratum radiatum, 40% in s. oriens, and 10% in s. lacunosum-moleculare. Juvenile cells had a rather higher proportion (20%) in s. lacunosum-moleculare. In general, some 50% of all spines were located within a path length of 200 microns from the soma. These total numbers of spines were much higher than earlier values from Golgi-impregnated cells but align well with estimates of the numbers of axonal boutons supplied to CA1 by CA3 pyramidal cells.
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              Age and hemisphere effects on dendritic structure.

              The dendritic structures of 187 small supragranular pyramidal neurons of the posterior superior temporal gyrus were studied with rapid Golgi impregnations in postmortem samples from 10 men aged 21-71 years. The number of primary basilar dendritic branches, the total number of basilar dendritic endings, the total basilar dendritic length, the total number of visible basilar dendritic spines and the cell soma sizes were all positively inter-correlated and all features were correlated to age (r = -0.77, -0.88, -0.82, -0.72, -0.86, respectively; all P < 0.05). These neuronal measures all correlated with brain weight (r = 0.79*, 0.65*, 0.51, 0.45, 0.55, respectively; *denotes P < 0.05). A first principle component derived from the inter-correlations of the neuronal features plus brain weight correlated almost perfectly with age (r = -0.93). The neuronal features differed between the right and left hemispheres (Wilks' Lambda = 0.91, P < 0.01). Post hoc tests showed that the dendritic trees of the right hemisphere were longer (P = 0.002), more branched (P = 0.008) and possessed more dendritic spines (P = 0.0009; Sheffe's tests). In conclusion, there are hemispheric differences in the dendritic structure of the small pyramidal neurons of presumptive human speech cortex and its right hemisphere analogue. Generalized neuronal atrophy is highly correlated with both brain weight and age, and is a candidate process to explain the decline in cognition with age.
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                Author and article information

                Journal
                The Journal of Comparative Neurology
                J. Comp. Neurol.
                Wiley
                0021-9967
                1096-9861
                October 06 1997
                October 06 1997
                : 386
                : 4
                : 661-680
                Article
                10.1002/(SICI)1096-9861(19971006)386:4<661::AID-CNE11>3.0.CO;2-N
                9378859
                9c81a0ba-bbf0-40ea-a8ec-090e16b06a85
                © 1997

                http://doi.wiley.com/10.1002/tdm_license_1.1

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