Alterations in the somatodendritic structure of spiny neurons in human putamen during physiological aging

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Abstract

Introduction. The striatum is involved in regulation of cognitive functions and behavior, including planning motor behavior, decision making, motivation, and rewarding. The human striatum contains the putamen, in whose medium spiny neurons certain qualitative and quantitative alterations in somatodendritic structure occur with aging.

Materials and methods. The morphometric parameters of spiny neurons in the striatum of humans (females) during the second maturity period and senility were investigated. The Golgi silver impregnation method was used as the staining technique. The following parameters were assessed: the area of neuronal body, the number of dendrites, the number of free ends of all dendrites, the largest dendritic field radius, the total length of all dendrites, the dendritic field area, and the specific density of dendrites.

Results. It was demonstrated that in terms of soma size, the number of dendrites, the number of free ends of dendrites, and specific density of dendrites, there are negligible differences in spiny neurons in the putamen in humans of both ages in the samples under study. The parameters of the largest dendritic field radius, the total length of all dendrites and the dendritic field area for the senile individuals were significantly lower (p<0.05) than for the mature ones by 11, 13, and 15%, respectively. The total number of spines per 100 µm of dendrite in senile individuals was lower by 18% compared to that in women during the second period of maturity. The features of distribution of spines of different types over the putamen neurons in mature and senile individuals show the role played by mushroom-like spines in preservation and maintenance of synaptic connections required to ensure the elementary functions of putamen neurons.

Conclusions. Hence, we have demonstrated reduction in dendrite length and density of dendrite spines upon aging in women. The results broaden the views about the nature of plastic alterations that take place in cerebral neurons in humans upon aging.

About the authors

Mikhail V. Ivanov

Research Center of Neurology

Author for correspondence.
Email: putamen@list.ru
Russian Federation, Moscow

Kristina A. Kutukova

Research Center of Neurology

Email: putamen@list.ru
Russian Federation, Moscow

Larisa A. Berezhnaya

Research Center of Neurology

Email: putamen@list.ru
Russian Federation, Moscow

References

  1. Ashby F.G., Turner B.O., Horvitz J.C. Cortical and basal ganglia contributions to habit learning and automaticity. Trends Cg Sci. 2010; 14(5): 208-215. doi: 10.1016/j.tics.2010.02.001 PMID: 20207189
  2. Mizumori S., Puryear C.B., Martiga A.K. Basal ganglia contributions to adaptive navigation. Behav Brain Res. 2009; 199(1): 32-42. doi: 10.1016/j.bbr.2008.11.014 PMID: 19056429
  3. Yager L.M., Garcia A.F., Wunsch A.M., Ferguson S.M. The ins and outs of the striatum: Role in drug addiction. J Neurosci. 2015; 301: 529–541. doi: 10.1016/j.neuroscience.2015.06.033 PMID: 26116518
  4. Stancheva S.L., Alova L.G. Biogenic monoamine uptake by rat brain synaptosomes during aging effects of nootropic drugs. Gen. Pharmacol. 1994; 25(5): 981–987. PMID: 7835648
  5. Birkmayer J.G.D., Birkmayer W. Improvement of disability and akinesia of patients with Parkinson’s disease by intravenous substitution. Ann Clin & Lab Sci. 1987; 17(1): 32-35. PMID: 3579206
  6. Green C.R., Wilson C.J. The basal ganglia. In: Swanson L.W., Bjorklund A., Hokfelt T. (eds) Integrated systems of the CNS, Part III. Cerebellum, Basal ganglia, Olfactory system. Handbook of chemical neuroanatomy. Amsterdam: Elsevier, 1996. 12. 583 p.
  7. Nieuwenhuys R., Voogd J., Huijzen C. van. The Human Central Nervous System. Springer, 2008. 967 p. doi: 10.1007/978-3-540-34686-9
  8. Steiner H., Tseng K.Y. Handbook of basal ganglia structure and function. London: Academic, 2010. 704 p.
  9. Dickstein D.L., Weaver C.M., Luebke J.I., Hof P.R. Dendritic spine changes associated with normal aging. Neuroscience. 2013; 251: 21-32. doi: 10.1016/j.neuroscience.2012.09.077 PMID: 23069756
  10. Levine M.S., Adinolfi A.M., Fisher R.S. et al. Quantitative morphology of medium-sized caudate spiny neurons in aged cats. Neurobiology of aging. 1986; 7(4): 277-286. PMID: 3748270
  11. Itzev D.E., Lolova I., Lolov S., Usunoff K.G. Age-related changes in the synapses of the rat’s neostriatum. Arch Physiol Biochem. 2001; 109(1):80–89. doi: 10.1076/apab.109.1.80.4279 PMID: 11471075
  12. Leontovich T.A., Fedorov A.A., Mukhina J.K. et al. Neuron species and neuron categories of human striatum. Moscow: «Sputnik +». 2015. 132 p.
  13. Peters A., Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am J Anat. 1970; 127(4): 321-356.
  14. Pickel V.M., Segal M. The Synapse: Structure and Function. Elsevier, 2013. 512 p.
  15. Wilson, C., Groves, P., Kitai, S., Linder, J. Three-dimensional structure of dendritic spines in the rat neostriatum. J Neurosci. 1983; 3(2): 383-388.
  16. Dall'Oglio A., Dutra A.C., Jorge E., et al. The human medial amygdala: structure, diversity, and complexity of dendritic spines. Journal of Anatomy. 2015; 227(4): 440–459. doi: 10.1111/joa.12358 PMID: 26218827
  17. von Bossanyi P, Becher M. Quantitative study of the dendritic spins of lamina V pyramidal neurons of the frontal lobe in children with severe mental retardation. J Hirnforsch. 1990; 31(2):181–192. PMID: 2358662
  18. Young K.A., Thompson P.M., Cruz D.A. et al. BA11 FKBP5 expression levels correlate with dendritic spine density in postmortem PTSD and controls. Neurobiology of Stress. 2015; 2: 67–72. doi: 10.1016/j.ynstr.2015.07.002 PMID: 26844242
  19. Krstonošić B., Milošević N., Gudović R. et al. Neuronal images of the putamen in the adult human neostriatum: a revised classification supported by a qualitative and quantitative analysis. Anatomical Science International. 2012; 87(3):115-125. doi: 10.1007/s12565-012-0131-4 PMID: 22467038
  20. Graveland G.A, DiFiglia M. The frequency and distribution of medium-sized neurons indented nuclei in the primate and rodent neostriatum. Brain Res. 1985; 327(1-2):307–311 PMID: 3986508
  21. Duan H., Wearne S.L., Rocher A.B. et al. Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex. 2003; 13(9): 950-61. PMID: 12902394
  22. Jacobs B., Driscoll L., Schall M. Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol. 1997; 386(4):661–680. PMID: 9378859
  23. Mukhina Yu.K., Fedorov A.A. [Study of structural changes of neurons in adult human entorhinal cortex, layer two]. In: [Fundamental problems of neuroscience: functional asymmetry, neuroplasticity and neurodegeneration. Materials of the All-Russian Scientific Conference]. Moscow; 2014: 705-710. (in Russ.)
  24. Rubinow M.J., Drogos L.L., Juraska J.M. Age-related dendritic hypertrophy and sexual dimorphism in rat basolateral amygdala. Neurobiol Aging. 2009; 30(1):137–146. doi: 10.1016/j.neurobiolaging.2007.05.006 PMID: 17570563
  25. Nakamura S., Akiguchi I., Kameyama M., Mizuno N. Age-related changes of pyramidal cell basal dendrites in layers III and V of human motor cortex: a quantitative Golgi study. Acta Neuropathol. 1985; 65(3-4):281–284. PMID: 3976364
  26. Scheibel M.E., Lindsay R.D., Tomiyasu U., Scheibel A.B. Progressive dendritic changes in aging human cortex. Exp Neurol. 1975; 47(3):392–403. PMID: 48474
  27. Cruz-Sanchez F.F., Cardozo A., Tolosa E. Neuronal changes in the substantia nigra with aging: a Golgi study. J Neuropathol Exp Neurol. 1995; 54(1):74–81. PMID: 7815082
  28. Cupp C.J., Uemura E. Age-related changes in prefrontal cortex of Macaca mulatta: quantitative analysis of dendritic branching patterns. Exp Neurol. 1980; 69(1):143–163. PMID: 6771151
  29. Dumitriu D., Hao J., Hara Y. et al. Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J Neurosci. 2010; 30(22):7507–7515. doi: 10.1523/JNEUROSCI.6410-09.2010 PMID: 20519525
  30. Geinisman Y., deToledo-Morrell L., Morrell F. et al. Age-related loss of axospinous synapses formed by two afferent systems in the rat dentate gyrus as revealed by the unbiased stereological dissector technique. Hippocampus. 1992; 2(4): 437–444. doi: 10.1002/hipo.450020411 PMID: 1308200
  31. Itzev D.E, Lolov S.R, Usunoff K.G. Aging and synaptic changes in the paraventricular hypothalamic nucleus of the rat. Acta Physiol Pharmacol Bulg. 2003; 27(2-3):75–82. PMID: 14570152
  32. Arellano J.I., Benavides-Piccione R., DeFelipe J., Yuste R. Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci. 2007; 1(1): 131-143. doi: 10.3389/neuro.01.1.1.010.2007 PMID: 18982124
  33. Spacek, J. and Hartmann, M. Three-dimensional analysis of dendritic spines. Quantitative observations related to dendritic spine and synaptic morphology in cerebral and cerebellar cortices Anat Embryol. 1983; 167(2): 289-310. PMID: 6614508

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Copyright (c) 2017 Ivanov M.V., Kutukova K.A., Berezhnaya L.A.

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