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Neurogenesis in the Adult Mammalian Brain

Yıl 2017, Sayı: 2, 70 - 88, 05.09.2017

Öz

It is currently
accepted that two regions of the adult mammalian brain continue to generate new
neurons throughout life. The subventricular zone (SVZ) of the lateral
ventricles gives rise to new neurons that migrate to the olfactory bulb to
become new interneurons, and the subgranular zone (SGZ) of the hippocampal dentate
gyrus (DG) generates new granule cells. Newborn neurons have distinct
morphological and functional properties that contribute to certain brain
functions which distinguishes them from the surrounding older neurons.
Persistent neurogenesis in the adult brain occurs in many mammalian species,
presenting certain species-specific differentiations. Differences in the rate
of adult hippocampal neurogenesis are also observed along the hippocampal
septo-temporal axis.



The present review
aims a. to present the features of the multistep adult neurogenesis process in
the SVZ and SGZ, b. to identify the unique characteristics of these two
neurogenic regions of the adult mammalian brain, and c. to comparatively
evaluate existing knowledge on neurogenesis similarities and differences among
evolutionary different mammalian species, trying to relate brain structure and
function with perpetual plasticity.



Adult neurogenesis
is a dynamic and complex process that promotes brain’s plasticity under normal
and pathological conditions. The comparative study of adult neurogenesis in
mammalian species with phylogenetic proximity to humans, strengthens our
knowledge in the field and creates unique opportunities for future novel
therapeutics.  

Kaynakça

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  • 2. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci. 1999;19(19):8487-97.
  • 3. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell. 2008;132(4):645-60.
  • 4. Kempermann G. Adult Hippocampal Neurogenesis. Adult Neurogenesis 2. New York: Oxford University Press, 2011. p. 185-215.
  • 5. Kuwabara T, Hsieh J, Muotri A, Yeo G, Warashina M, Lie DC, Moore L, Nakashima K, Asashima M, Gage FH. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci. 2009;12(9):1097-105.
  • 6. Shetty AK, Hattiangady B, Shetty GA. Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia. 2005;51(3):173-86.
  • 7. Jiao J, Chen DF. Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells. 2008;26(5):1221-30.
  • 8. Krzisch M, Temprana SG, Mongiat LA, Armida J, Schmutz V, Virtanen MA, Kocher-Braissant J, Kraftsik R, Vutskits L, Conzelmann KK, Bergami M, Gage FH, Schinder AF, Toni N. Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus. Brain Struct Funct. 2015; 220(4):2027–2042.
  • 9. Hellsten J, Wennstrom M, Bengzon J, Mohapel P, Tingstrom A. Electroconvulsive seizures induce endothelial cell proliferation in adult rat hippocampus. Biol Psychiatry. 2004;55(4):420-7.
  • 10. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet. 2004;36(8):827-35.
  • 11. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol. 2000;425(4):479-94.
  • 12. Alvarez-Buylla A, Kohwi M, Nguyen TM, Merkle FT. The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb Symp Quant Biol. 2008;73:357-65.
  • 13. Gubert F, Zaverucha-do-Valle C, Pimentel-Coelho PM, Mendez-Otero R, Santiago MF. Radial glia-like cells persist in the adult rat brain. Brain Res. 2009;1258:43-52.
  • 14. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 1997;17(13):5046-61.
  • 15. Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol. 1998;36(2):234-48.
  • 16. Lledo PM, Saghatelyan A. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 2005;28(5):248-54.
  • 17. Lledo PM, Alonso M, Grubb MS. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci. 2006;7(3):179-93.
  • 18. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci. 2006;26(30):7907-18.
  • 19. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Baron-Van Evercooren A. The role of SVZ-derived neural precursors in demyelinating diseases: from animal models to multiple sclerosis. J Neurol Sci. 2008;265(1-2):26-31.
  • 20. Gage FH. Mammalian neural stem cells. Science. 2000;287(5457):1433-8.
  • 21. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci. 2001;21(18):7153-60.
  • 22. Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, Yamaguchi M, Kettenmann H, Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci. 2003;23(3):373-82.
  • 23. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 2004;27(8):447-52.
  • 24. von Bohlen und Halbach O. Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Res. 2011;345(1):1-19.
  • 25. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol. 2004;478(4):359-78.
  • 26. Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, Kempermann G. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia. 2006;54(8):805-14.
  • 27. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature. 2006;439(7076):589-93.
  • 28. Piatti VC, Esposito MS, Schinder AF. The timing of neuronal development in adult hippocampal neurogenesis. Neuroscientist. 2006;12(6):463-8.
  • 29. Steiner B, Kronenberg G, Jessberger S, Brandt MD, Reuter K, Kempermann G. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia. 2004;46(1):41-52.
  • 30. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, von der Behrens W, Kempermann G. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci. 2003;24(3):603-13.
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  • 32. Liu Y, Fujise N, Kosaka T. Distribution of calretinin immunoreactivity in the mouse dentate gyrus. I. General description. Exp Brain Res. 1996;108(3):389-403.
  • 33. Duan X, Kang E, Liu CY, Ming GL, Song H. Development of neural stem cell in the adult brain. Curr Opin Neurobiol. 2008;18(1):108-15.
  • 34. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science. 2009;325(5937):210-3.
  • 35. Tronel S, Belnoue L, Grosjean N, Revest JM, Piazza PV, Koehl M, Abrous DN. Adult-born neurons are necessary for extended contextual discrimination. Hippocampus. 2010;22(2):292-8.
  • 36. Brunne B, Zhao S, Derouiche A, Herz J, May P, Frotscher M, Bock HH. Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Glia. 2010;58(13):1553-69.
  • 37. Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, Peterson DA, Fishell G, Koulakov A, Enikolopov G. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell. 2011;8(5):566-79.
  • 38. Morrens J, Van Den Broeck W, Kempermann G. Glial cells in adult neurogenesis. Glia. 2012;60(2):159-74.
  • 39. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN. Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci. 1999;113(6):1170-88.
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  • 41. Grivas I, Michaloudi H, Batzios C, Chiotelli M, Papatheodoropoulos C, Kostopoulos G, Papadopoulos GC. Vascular network of the rat hippocampus is not homogeneous along the septotemporal axis. Brain Res. 2003;971(2):245-9.
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  • 43. Snyder JS, Ferrante SC, Cameron HA. Late maturation of adult-born neurons in the temporal dentate gyrus. PLoS One. 2012;7(11):e48757.
  • 44. Amrein I, Dechmann DKN, Winter Y, Lipp HP. Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera). PLoS One. 2007;2(e455).
  • 45. Bartkowksa K, Djavadian RL, Taylor JRE, Turlejski K. Generation recruitment and death of brain cells throught the life cycle of Sorex shrews (Lipotyphla). Eur J Neurosci. 2008;27:1710-21.
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  • 47. Kempermann G, Kuhn HG, Gage FH. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci U S A. 1997;94(19):10409-14.
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Erişkin Memeli Beyninde Neurogenesis

Yıl 2017, Sayı: 2, 70 - 88, 05.09.2017

Öz

Günümüzde, erişkin memeli
beyninin iki bölgesinde, yaşam boyunca yeni nöronların üretilmeye devam ettiği
kabul edilmektedir. Ventriculus lateralis’in zona subventricularis’i (SVZ)
tarafından üretilen yeni nöronlar, bulbus olfactorius’a göç ederek yeni
internöronların oluşumuna neden olur. Bunun dışında hippocampus’un gyrus
dentatus’unun  (DG) zona subgranularis’i  (SGZ), yeni granüler hücreler üretir.



Yeni oluşan nöronlar,  belirli beyin fonksiyonlarına katkıda bulunan
ve onları çevreleyen daha eski nöronlardan ayıran, belirgin morfolojik ve
fonksiyonel özelliklere sahiptir.

Birçok memeli türünün erişkin beyninde, 
bazı türlere özgü farklılıklar göstermekle birlikte, kalıcı neurogenesis
şekillenir. Erişkin hippokampal neurogenesis hızındaki farklılıklar,
hippocampus’un axis septo-temporalis’inde de gözlenmektedir.



Bu derlemede; a. SVZ ve SGZ'da çok basamaklı
erişkin neurogenesis sürecinin özelliklerini sunmak, b. erişkin memeli beyninin
bu iki neurogenic bölgesinin benzersiz özelliklerini tanımlamak ve c. evrimsel
olarak farklı memeli türleri arasındaki neurogenesis benzerlikleri ve
farklılıkları hakkındaki mevcut bilgileri karşılaştırarak değerlendirmek, beyin
yapısı ve işleyişini kalıcı plastisite ile ilişkilendirmeye çalışmak
amaçlanmıştır.

Erişkin neurogenesis, normal ve patolojik koşullar altında beyin plastisitesini
yükselten dinamik ve kompleks bir süreçtir. Filogenetik olarak insanlara
yakınlığı olan memeli türlerinde yapılan karşılaştırmalı yetişkin neurogenesis
çalışmaları, bu alanla ilgili bilgilerimizi güçlendirmekte ve gelecekte
oluşturulabilecek yeni terapötikler için eşsiz fırsatlar yaratmaktadır.

Kaynakça

  • 1. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol. 1965;124(3):319-36.
  • 2. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci. 1999;19(19):8487-97.
  • 3. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell. 2008;132(4):645-60.
  • 4. Kempermann G. Adult Hippocampal Neurogenesis. Adult Neurogenesis 2. New York: Oxford University Press, 2011. p. 185-215.
  • 5. Kuwabara T, Hsieh J, Muotri A, Yeo G, Warashina M, Lie DC, Moore L, Nakashima K, Asashima M, Gage FH. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci. 2009;12(9):1097-105.
  • 6. Shetty AK, Hattiangady B, Shetty GA. Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia. 2005;51(3):173-86.
  • 7. Jiao J, Chen DF. Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells. 2008;26(5):1221-30.
  • 8. Krzisch M, Temprana SG, Mongiat LA, Armida J, Schmutz V, Virtanen MA, Kocher-Braissant J, Kraftsik R, Vutskits L, Conzelmann KK, Bergami M, Gage FH, Schinder AF, Toni N. Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus. Brain Struct Funct. 2015; 220(4):2027–2042.
  • 9. Hellsten J, Wennstrom M, Bengzon J, Mohapel P, Tingstrom A. Electroconvulsive seizures induce endothelial cell proliferation in adult rat hippocampus. Biol Psychiatry. 2004;55(4):420-7.
  • 10. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet. 2004;36(8):827-35.
  • 11. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol. 2000;425(4):479-94.
  • 12. Alvarez-Buylla A, Kohwi M, Nguyen TM, Merkle FT. The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb Symp Quant Biol. 2008;73:357-65.
  • 13. Gubert F, Zaverucha-do-Valle C, Pimentel-Coelho PM, Mendez-Otero R, Santiago MF. Radial glia-like cells persist in the adult rat brain. Brain Res. 2009;1258:43-52.
  • 14. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 1997;17(13):5046-61.
  • 15. Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol. 1998;36(2):234-48.
  • 16. Lledo PM, Saghatelyan A. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 2005;28(5):248-54.
  • 17. Lledo PM, Alonso M, Grubb MS. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci. 2006;7(3):179-93.
  • 18. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci. 2006;26(30):7907-18.
  • 19. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Baron-Van Evercooren A. The role of SVZ-derived neural precursors in demyelinating diseases: from animal models to multiple sclerosis. J Neurol Sci. 2008;265(1-2):26-31.
  • 20. Gage FH. Mammalian neural stem cells. Science. 2000;287(5457):1433-8.
  • 21. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci. 2001;21(18):7153-60.
  • 22. Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, Yamaguchi M, Kettenmann H, Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci. 2003;23(3):373-82.
  • 23. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 2004;27(8):447-52.
  • 24. von Bohlen und Halbach O. Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Res. 2011;345(1):1-19.
  • 25. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol. 2004;478(4):359-78.
  • 26. Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, Kempermann G. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia. 2006;54(8):805-14.
  • 27. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature. 2006;439(7076):589-93.
  • 28. Piatti VC, Esposito MS, Schinder AF. The timing of neuronal development in adult hippocampal neurogenesis. Neuroscientist. 2006;12(6):463-8.
  • 29. Steiner B, Kronenberg G, Jessberger S, Brandt MD, Reuter K, Kempermann G. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia. 2004;46(1):41-52.
  • 30. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, von der Behrens W, Kempermann G. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci. 2003;24(3):603-13.
  • 31. Bekiari C, Giannakopoulou A, Siskos N, Grivas I, Tsingotjidou A, Michaloudi H, Papadopoulos GC. Neurogenesis in the septal and temporal part of the adult rat dentate gyrus. Hippocampus. 2015;25(4):511-23.
  • 32. Liu Y, Fujise N, Kosaka T. Distribution of calretinin immunoreactivity in the mouse dentate gyrus. I. General description. Exp Brain Res. 1996;108(3):389-403.
  • 33. Duan X, Kang E, Liu CY, Ming GL, Song H. Development of neural stem cell in the adult brain. Curr Opin Neurobiol. 2008;18(1):108-15.
  • 34. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science. 2009;325(5937):210-3.
  • 35. Tronel S, Belnoue L, Grosjean N, Revest JM, Piazza PV, Koehl M, Abrous DN. Adult-born neurons are necessary for extended contextual discrimination. Hippocampus. 2010;22(2):292-8.
  • 36. Brunne B, Zhao S, Derouiche A, Herz J, May P, Frotscher M, Bock HH. Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Glia. 2010;58(13):1553-69.
  • 37. Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, Peterson DA, Fishell G, Koulakov A, Enikolopov G. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell. 2011;8(5):566-79.
  • 38. Morrens J, Van Den Broeck W, Kempermann G. Glial cells in adult neurogenesis. Glia. 2012;60(2):159-74.
  • 39. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN. Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci. 1999;113(6):1170-88.
  • 40. Fanselow MS, Dong HW. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron. 2010;65(1):7-19.
  • 41. Grivas I, Michaloudi H, Batzios C, Chiotelli M, Papatheodoropoulos C, Kostopoulos G, Papadopoulos GC. Vascular network of the rat hippocampus is not homogeneous along the septotemporal axis. Brain Res. 2003;971(2):245-9.
  • 42. Wu MV, Hen R. Functional dissociation of adult-born neurons along the dorsoventral axis of the dentate gyrus. Hippocampus. 2014;24(7):751-61.
  • 43. Snyder JS, Ferrante SC, Cameron HA. Late maturation of adult-born neurons in the temporal dentate gyrus. PLoS One. 2012;7(11):e48757.
  • 44. Amrein I, Dechmann DKN, Winter Y, Lipp HP. Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera). PLoS One. 2007;2(e455).
  • 45. Bartkowksa K, Djavadian RL, Taylor JRE, Turlejski K. Generation recruitment and death of brain cells throught the life cycle of Sorex shrews (Lipotyphla). Eur J Neurosci. 2008;27:1710-21.
  • 46. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci. 2009;29(46):14484-95.
  • 47. Kempermann G, Kuhn HG, Gage FH. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci U S A. 1997;94(19):10409-14.
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  • 61. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4(11):1313-7.
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Toplam 67 adet kaynakça vardır.

Ayrıntılar

Konular Klinik Tıp Bilimleri
Bölüm Makaleler
Yazarlar

Chryssa Bekıarı Bu kişi benim

Rıfat Mutuş

Georgios C. Papadopoulos

Yayımlanma Tarihi 5 Eylül 2017
Kabul Tarihi 12 Haziran 2017
Yayımlandığı Sayı Yıl 2017 Sayı: 2

Kaynak Göster

JAMA Bekıarı C, Mutuş R, Papadopoulos GC. Neurogenesis in the Adult Mammalian Brain. IGUSABDER. 2017;:70–88.

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