دورية أكاديمية

Adult-Born Hippocampal Neurons Undergo Extended Development and Are Morphologically Distinct from Neonatally-Born Neurons.

التفاصيل البيبلوغرافية
العنوان: Adult-Born Hippocampal Neurons Undergo Extended Development and Are Morphologically Distinct from Neonatally-Born Neurons.
المؤلفون: Cole JD; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada., Espinueva DF; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada., Seib DR; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada., Ash AM; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada., Cooke MB; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada., Cahill SP; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada., O'Leary TP; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada., Kwan SS; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada., Snyder JS; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada jasonsnyder@psych.ubc.ca.
المصدر: The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2020 Jul 22; Vol. 40 (30), pp. 5740-5756. Date of Electronic Publication: 2020 Jun 22.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Society for Neuroscience Country of Publication: United States NLM ID: 8102140 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1529-2401 (Electronic) Linking ISSN: 02706474 NLM ISO Abbreviation: J Neurosci Subsets: MEDLINE
أسماء مطبوعة: Publication: Washington, DC : Society for Neuroscience
Original Publication: [Baltimore, Md.] : The Society, c1981-
مواضيع طبية MeSH: Hippocampus/*cytology , Hippocampus/*growth & development , Neurogenesis/*physiology , Neuronal Plasticity/*physiology , Neurons/*physiology, Age Factors ; Animals ; Animals, Newborn ; Male ; Maze Learning/physiology ; Rats ; Rats, Long-Evans
مستخلص: During immature stages, adult-born neurons pass through critical periods for survival and plasticity. It is generally assumed that by 2 months of age adult-born neurons are mature and equivalent to the broader neuronal population, raising questions of how they might contribute to hippocampal function in old age when neurogenesis has declined. However, few have examined adult-born neurons beyond the critical period or directly compared them to neurons born in infancy. Here, we used a retrovirus to visualize functionally relevant morphological features of 2- to 24-week-old adult-born neurons in male rats. From 2 to 7 weeks, neurons grew and attained a relatively mature phenotype. However, several features of 7-week-old neurons suggested a later wave of growth: these neurons had larger nuclei, thicker dendrites, and more dendritic filopodia than all other groups. Indeed, between 7 and 24 weeks, adult-born neurons gained additional dendritic branches, formed a second primary dendrite, acquired more mushroom spines, and had enlarged mossy fiber presynaptic terminals. Compared with neonatal-born neurons, old adult-born neurons had greater spine density, larger presynaptic terminals, and more putative efferent filopodial contacts onto inhibitory neurons. By integrating rates of cell birth and growth across the life span, we estimate that adult neurogenesis ultimately produces half of the cells and the majority of spines in the dentate gyrus. Critically, protracted development contributes to the plasticity of the hippocampus through to the end of life, even after cell production declines. Persistent differences from neonatal-born neurons may additionally endow adult-born neurons with unique functions even after they have matured. SIGNIFICANCE STATEMENT Neurogenesis occurs in the hippocampus throughout adult life and contributes to memory and emotion. It is generally assumed that new neurons have the greatest impact on behavior when they are immature and plastic. However, since neurogenesis declines dramatically with age, it is unclear how they might contribute to behavior later in life when cell proliferation has slowed. Here we find that newborn neurons mature over many months in rats and may end up with distinct morphological features compared with neurons born in infancy. Using a mathematical model, we estimate that a large fraction of neurons is added in adulthood. Moreover, their extended growth produces a reserve of plasticity that persists even after neurogenesis has declined to low rates.
(Copyright © 2020 the authors.)
References: Nature. 2011 May 26;473(7348):514-8. (PMID: 21532590)
J Comp Neurol. 1981 Jan 1;195(1):51-86. (PMID: 7204652)
J Neurosci. 1996 Mar 15;16(6):2027-33. (PMID: 8604047)
J Neurosci. 2006 Jan 4;26(1):3-11. (PMID: 16399667)
Nat Neurosci. 2008 Aug;11(8):901-7. (PMID: 18622400)
Neurobiol Aging. 1987 Nov-Dec;8(6):521-45. (PMID: 3323927)
eNeuro. 2015 Sep 28;2(5):. (PMID: 26478908)
Nature. 2004 May 13;429(6988):184-7. (PMID: 15107864)
Brain Res. 1985 Oct 21;345(2):366-8. (PMID: 4041896)
J Neurosci. 2014 Feb 5;34(6):2349-54. (PMID: 24501373)
Proc Natl Acad Sci U S A. 2010 Jul 13;107(28):12687-91. (PMID: 20616040)
Science. 2016 Oct 28;354(6311):459-465. (PMID: 27789840)
PLoS One. 2009;4(4):e5320. (PMID: 19399173)
J Comp Neurol. 1990 Dec 8;302(2):206-19. (PMID: 2289972)
Prog Brain Res. 2007;163:63-84. (PMID: 17765712)
Anat Rec. 1991 Dec;231(4):482-97. (PMID: 1793176)
Brain Behav. 2019 Oct;9(10):e01435. (PMID: 31576673)
Science. 2012 Mar 9;335(6073):1238-42. (PMID: 22282476)
PLoS One. 2012;7(9):e45270. (PMID: 23024813)
Nat Neurosci. 2002 Aug;5(8):790-5. (PMID: 12118256)
Brain Res. 2010 Apr 30;1328:12-24. (PMID: 20206610)
Proc Natl Acad Sci U S A. 2018 May 15;115(20):E4670-E4679. (PMID: 29712871)
Behav Brain Res. 2010 Dec 31;215(2):180-96. (PMID: 20307583)
Hippocampus. 2011 Dec;21(12):1348-62. (PMID: 20824726)
J Neurosci. 2008 Feb 6;28(6):1374-84. (PMID: 18256257)
Proc Natl Acad Sci U S A. 1986 May;83(9):3027-31. (PMID: 3458260)
Neuroscience. 1993 Sep;56(2):337-44. (PMID: 8247264)
Brain Behav Immun. 2016 Mar;53:242-254. (PMID: 26724574)
Neurosci Bull. 2015 Dec;31(6):685-96. (PMID: 26345180)
J Neurosci. 2011 May 25;31(21):7715-28. (PMID: 21613484)
Brain Struct Funct. 2018 Sep;223(7):3213-3228. (PMID: 29796923)
J Neurosci. 2013 Jul 10;33(28):11400-11. (PMID: 23843512)
Nat Protoc. 2020 Feb;15(2):668-693. (PMID: 31915385)
Neuroscience. 2007 Oct 26;149(2):273-85. (PMID: 17900815)
J Comp Neurol. 1965 Jun;124(3):319-35. (PMID: 5861717)
J Comp Neurol. 1992 Nov 8;325(2):169-82. (PMID: 1460112)
Neuron. 2017 Sep 27;96(1):43-55. (PMID: 28957675)
Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):7963-8. (PMID: 20375283)
Hippocampus. 2013 Aug;23(8):708-19. (PMID: 23554226)
Prog Brain Res. 2007;163:43-61. (PMID: 17765711)
Nat Rev Neurosci. 2009 Sep;10(9):647-58. (PMID: 19693029)
Trends Neurosci. 2015 Dec;38(12):800-812. (PMID: 26607684)
Elife. 2016 Oct 25;5:. (PMID: 27780032)
PLoS Comput Biol. 2016 May 04;12(5):e1004897. (PMID: 27145441)
Transl Psychiatry. 2011 Aug 30;1:e35. (PMID: 22832609)
Trends Neurosci. 2019 Mar;42(3):164-178. (PMID: 30686490)
Eur J Neurosci. 2011 Jan;33(1):175-81. (PMID: 21143670)
J Comp Neurol. 2003 Jun 9;460(4):563-72. (PMID: 12717714)
J Neurosci. 2015 Jul 22;35(29):10600-12. (PMID: 26203153)
PLoS One. 2015 Aug 12;10(8):e0135493. (PMID: 26267362)
Neuron. 2015 Feb 18;85(4):710-7. (PMID: 25661179)
Behav Brain Res. 2012 Feb 14;227(2):470-9. (PMID: 21801754)
Hippocampus. 2017 Nov;27(11):1155-1167. (PMID: 28686814)
Nat Med. 2018 May;24(4):438-449. (PMID: 29529016)
Sci Rep. 2017 Aug 21;7(1):8877. (PMID: 28827727)
Front Neurosci. 2018 Oct 05;12:706. (PMID: 30344473)
Nat Neurosci. 2007 Jun;10(6):727-34. (PMID: 17486101)
J Neurophysiol. 2001 Jun;85(6):2423-31. (PMID: 11387388)
Neuroimage. 2016 May 1;131:29-41. (PMID: 26589333)
Nat Neurosci. 2012 Dec;15(12):1700-6. (PMID: 23143513)
Nat Neurosci. 2016 Jun;19(6):788-91. (PMID: 27135217)
J Neurosci. 2007 Aug 29;27(35):9400-7. (PMID: 17728453)
J Comp Neurol. 1975 Jan 15;159(2):149-75. (PMID: 1112911)
Neuron. 2016 Jul 20;91(2):370-83. (PMID: 27346528)
Neuron. 2010 Mar 11;65(5):627-42. (PMID: 20223199)
Hippocampus. 2019 Jun;29(6):539-549. (PMID: 30365199)
J Neurosci. 2007 Mar 21;27(12):3252-9. (PMID: 17376985)
Neuron. 2006 Jun 1;50(5):749-63. (PMID: 16731513)
Neuron. 2007 May 24;54(4):559-66. (PMID: 17521569)
J Neurosci. 2012 Feb 29;32(9):3101-8. (PMID: 22378883)
J Neurosci. 2009 Nov 18;29(46):14484-95. (PMID: 19923282)
J Neurosci. 2013 Apr 10;33(15):6614-22. (PMID: 23575858)
Transl Psychiatry. 2014 Oct 14;4:e463. (PMID: 25313506)
J Neurosci. 2006 Feb 22;26(8):2326-34. (PMID: 16495460)
Proc Natl Acad Sci U S A. 2004 May 4;101(18):7181-6. (PMID: 15118105)
Proc Natl Acad Sci U S A. 2011 Jun 21;108(25):10326-31. (PMID: 21646517)
Elife. 2016 Oct 03;5:. (PMID: 27692065)
Nat Neurosci. 2008 Feb;11(2):178-86. (PMID: 18204443)
Neuron. 2005 Feb 3;45(3):405-17. (PMID: 15694327)
Neuron. 2006 Mar 16;49(6):861-75. (PMID: 16543134)
J Neurobiol. 2000 Feb 5;42(2):248-57. (PMID: 10640331)
J Comp Neurol. 1986 Apr 22;246(4):435-58. (PMID: 3700723)
J Neurosci. 1998 May 1;18(9):3386-403. (PMID: 9547246)
Nat Med. 2019 Apr;25(4):554-560. (PMID: 30911133)
Neurobiol Aging. 2012 Aug;33(8):1664-71. (PMID: 21621300)
Bioinformatics. 2011 Sep 1;27(17):2453-4. (PMID: 21727141)
PLoS Biol. 2006 Nov;4(12):e409. (PMID: 17121455)
Nat Commun. 2012;3:1253. (PMID: 23212382)
Trends Neurosci. 2008 Apr;31(4):163-9. (PMID: 18329110)
Nature. 2002 Feb 28;415(6875):1030-4. (PMID: 11875571)
Nat Rev Neurosci. 2008 Mar;9(3):206-21. (PMID: 18270515)
Epilepsy Res Suppl. 1992;7:3-28. (PMID: 1365013)
J Neurosci. 1991 Jun;11(6):1756-62. (PMID: 2045885)
J Neurosci. 2019 Feb 27;39(9):1605-1620. (PMID: 30651327)
J Comp Neurol. 1990 Mar 8;293(2):253-67. (PMID: 19189715)
Cereb Cortex. 2019 Jul 22;29(8):3527-3539. (PMID: 30215686)
Brain Struct Funct. 2015 Mar;220(2):645-61. (PMID: 24510284)
Brain Res. 2007 May 29;1149:30-7. (PMID: 16904657)
Cell Stem Cell. 2018 Jul 05;23(1):25-30. (PMID: 29681514)
Cereb Cortex. 2019 Jun 1;29(6):2639-2652. (PMID: 29878074)
Cell Stem Cell. 2018 Dec 6;23(6):780-781. (PMID: 30526879)
Hippocampus. 2016 Jun;26(6):763-78. (PMID: 26662922)
Behav Brain Funct. 2010 Jul 02;6:35. (PMID: 20594357)
J Neurosci. 2013 Dec 4;33(49):19131-42. (PMID: 24305810)
Nature. 2008 Mar 27;452(7186):436-41. (PMID: 18368112)
Proc Natl Acad Sci U S A. 2008 Sep 16;105(37):14157-62. (PMID: 18780780)
Neuron. 2009 Jan 29;61(2):187-202. (PMID: 19186162)
Brain Struct Funct. 2017 Apr;222(3):1427-1446. (PMID: 27514866)
J Neurosci. 2007 Sep 26;27(39):10434-44. (PMID: 17898215)
Hippocampus. 2010 Jul;20(7):799-810. (PMID: 19623538)
Behav Brain Res. 2012 Feb 14;227(2):384-90. (PMID: 21736900)
J Comp Neurol. 1983 Apr 1;215(2):154-64. (PMID: 6853770)
Cell Rep. 2017 Oct 31;21(5):1129-1139. (PMID: 29091753)
معلومات مُعتمدة: Canada CIHR
فهرسة مساهمة: Keywords: adult neurogenesis; aging; critical period; development; plasticity; retrovirus
تواريخ الأحداث: Date Created: 20200624 Date Completed: 20201225 Latest Revision: 20210122
رمز التحديث: 20240628
مُعرف محوري في PubMed: PMC7380968
DOI: 10.1523/JNEUROSCI.1665-19.2020
PMID: 32571837
قاعدة البيانات: MEDLINE
الوصف
تدمد:1529-2401
DOI:10.1523/JNEUROSCI.1665-19.2020