Reactive neurogenesis in response to naturally occurring apoptosis in an adult brain

Journal of Neuroscience

Volumn 34, Issue 39, 2014, Pages 13066-13076

  Larson, Tracy A ^a   Thatra, Nivretta M ^a   Lee, Brian H ^a,b   Brenowitz, Eliot A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Apoptosis; Neurogenesis; Neuronal turnover; Sex steroid; Song bird

Indexed keywords

BROXURIDINE; CASPASE 3; TESTOSTERONE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; APOPTOSIS; ARTICLE; BRAIN; BREEDING; CELL DEATH; CELL PROLIFERATION; CHROMATIN CONDENSATION; CONTROLLED STUDY; HISTOLOGY; HORMONE DETERMINATION; IMMUNOHISTOCHEMISTRY; MALE; MORPHOLOGY; NERVE CELL DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHYSIOLOGICAL PROCESS; SENSORIMOTOR FUNCTION; STEM CELL; TURNOVER TIME; ZONOTRICHIA LEUCOPHRYS; ZONOTRICHIA LEUCOPHRYS GAMBELII; ANIMAL; CYTOLOGY; FEMALE; GROWTH, DEVELOPMENT AND AGING; NERVE CELL; NEURAL STEM CELL; PHYSIOLOGY; SEASON; SPARROW; VOCALIZATION;

ANIMALS; APOPTOSIS; BRAIN; CELL PROLIFERATION; FEMALE; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; SEASONS; SPARROWS; VOCALIZATION, ANIMAL;

EID: 84907284543     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3316-13.2014     Document Type: Article

References (47)

1. Alvarez-Borda B, Nottebohm F (2002) Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. J Neurosci 22:8684-8690. Medline
2. Alvarez-Buylla A, Nottebohm F (1988) Migration of young neurons in adult avian brain. Nature 335:353-354. CrossRef Medline
3. Barami K, Iversen K, Furneaux H, Goldman SA (1995) Hu protein as an early marker of neuronal phenotypic differentiation by subependymal zone cells of the adult songbird forebrain. J Neurobiol 28:82-101. CrossRef Medline
4. Brenowitz EA (2008) Plasticity of the song control system in adult birds. In: Neuroscience of birdsong (Zeigler HP, Marler P, eds), pp 332-349. Cambridge: Cambridge UP.
5. Brown SD, Johnson F, Bottjer SW (1993) Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels. J Neurosci 13: 2024-2032. Medline
6. Chen BY, Wang X, Wang ZY, Wang YZ, Chen LW, Luo ZJ (2013) Brainderived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/β-catenin signaling pathway. J Neurosci Res 91:30-41. CrossRef Medline
7. Cho KO, Kim SY (2010) Effects of brain insults and pharmacological manipulations on the adult hippocampal neurogenesis. Arch Pharm Res 33:1475-1488. CrossRef Medline
8. Gage FH, Kempermann G, Song H (2008) Adult neurogenesis. Cold Spring Harbor: Cold Spring Harbor Laboratory.
9. Grote HE, Hannan AJ (2007) Regulators of adult neurogenesis in the healthy and diseased brain. Clin Exp Pharmacol Physiol 34:533-545. CrossRef Medline
10. Kim WR, Sun W (2011) Programmed cell death during postnatal development of the rodent nervous system. Dev Growth Differ 53:225-235. CrossRef Medline
11. Kirn JR, Alvarez-Buylla A, Nottebohm F (1991) Production and survival of projection neurons in a forebrain vocal center of adult male canaries. J Neurosci 11:1756 -1762. Medline
12. Kirn J, O'Loughlin B, Kasparian S, Nottebohm F (1994) Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. Proc Natl Acad Sci U S A 91:7844- 7848. CrossRef Medline
13. Kizil C, Kyritsis N, Dudczig S, Kroehne V, Freudenreich D, Kaslin J, BrandM (2012) Regenerative neurogenesis from neural progenitor cells requires injury-induced expression of gata3. Dev Cell 23:1230 -1237. CrossRef Medline
14. Kohman RA, Rhodes JS (2013) Neurogenesis, inflammation and behavior. Brain Behav Immun 27:22-32. CrossRef Medline
15. Kroehne V, Freudenreich D, Hans S, Kaslin J, BrandM (2011) Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors. Development 138:4831- 4841. CrossRef Medline
16. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033. Medline
17. Larson TA, Wang TW, Gale SD, Miller KE, Thatra NM, Caras ML, Perkel DJ, Brenowitz EA (2013) Postsynaptic neural activity regulates neuronal addition in the adult avian song control system. Proc Natl Acad Sci U S A 110:16640 -16644. CrossRef Medline
18. Leuner B, Kozorovitskiy Y, Gross CG, Gould E (2007) Diminished adult neurogenesis in the marmoset brain precedes old age. Proc Natl Acad Sci U S A 104:17169 -17173. CrossRef Medline
19. Li XC, Jarvis ED, Alvarez-Borda B, Lim DA, Nottebohm F (2000) A relationship between behavior, neurotrophin expression, and new neuron survival. Proc Natl Acad Sci U S A 97:8584-8589. CrossRef Medline
20. Mc Allister AK (2002) Neurotrophins and cortical development. Results Probl Cell Differ 39:89 -112. CrossRef Medline
21. Meitzen J, Thompson CK, Choi H, Perkel DJ, Brenowitz EA (2009) Time course of changes in Gambel's white-crowned sparrow song behavior following transitions in breeding condition. Horm Behav 55:217-227. CrossRef Medline
22. Molowny A, Nacher J, Lopez-Garcia C (1995) Reactive neurogenesis during regeneration of the lesioned medial cerebral cortex of lizards. Neuroscience 68:823- 836. CrossRef Medline
23. Pytte CL, Gerson M, Miller J, Kirn JR (2007) Increasing stereotypy in adult zebra finch song correlates with a declining rate of adult neurogenesis. Dev Neurobiol 67:1699 -1720. CrossRef Medline
24. Pytte C, Yu YL, Wildstein S, George S, Kirn JR (2011) Adult neuron addition to the zebra finch song motor pathway correlates with the rate and extent of recovery from Botox-induced paralysis of the vocal muscles. J Neurosci 31:16958 -16968. CrossRef Medline
25. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Güntürkün O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, et al. (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377- 414. CrossRef Medline
26. Riddle DR, Lichtenwalner RJ (2007) Neurogenesis in the adult and aging brain. In: Brain aging: models, methods, and mechanisms, Chap 6 (Riddle DR, ed). Boca Raton, FL: CRC Press.
27. Scharff C, Kirn JR, Grossman M, Macklis JD, Nottebohm F (2000) Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron 25:481- 492. CrossRef Medline
28. Scott BB, Lois C (2007) Developmental origin and identity of song system neurons born during vocal learning in songbirds. J Comp Neurol 502: 202-214. CrossRef Medline
29. Scott BB, Gardner T, Ji N, Fee MS, Lois C (2012) Wandering neuronal migration in the postnatal vertebrate forebrain. J Neurosci 32:1436 -1446. CrossRef Medline
30. Scotto-Lomassese S, Rochefort C, Nshdejan A, Scharff C (2007) HVC interneurons are not renewed in adult male zebra finches. Eur J Neurosci 25:1663-1668. CrossRef Medline
31. Smith GT, Brenowitz EA, Wingfield JC, Baptista LF (1995) Seasonal changes in song nuclei and song behavior in Gambel's white-crowned sparrows. J Neurobiol 28:114 -125. CrossRef Medline
32. Smith GT, Brenowitz EA, Wingfield JC (1997a) Seasonal changes in the size of the avian song control nucleus HVC defined by multiple histological markers. J Comp Neurol 381:253-261. CrossRef Medline
33. Smith GT, Brenowitz EA, Wingfield JC (1997b) Roles of photoperiod and testosterone in seasonal plasticity of the avian song control system. J Neurobiol 32:426-442. CrossRef Medline
34. Smith JA, Das A, Ray SK, Banik NL (2012) Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull 87:10 -20. CrossRef Medline
35. Srinivasan A, Roth KA, Sayers RO, Shindler KS, Wong AM, Fritz LC, Tomaselli KJ (1998) In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ 5:1004 -1016. CrossRef Medline
36. Thompson CK, Brenowitz EA (2008) Caspase inhibitor infusion protects an avian song control circuit from seasonal-like neurodegeneration. J Neurosci 28:7130 -7136. CrossRef Medline
37. Thompson CK, Brenowitz EA (2009) Neurogenesis in an adult avian song nucleus is reduced by decreasing caspase-mediated apoptosis. J Neurosci 29:4586-4591. CrossRef Medline
38. Thompson CK, Bentley GE, Brenowitz EA (2007) Rapid seasonal-like regression of the adult avian song control system. Proc Natl Acad Sci U S A 104:15520 -15525. CrossRef Medline
39. Thompson CK, Meitzen J, Replogle K, Drnevich J, Lent KL, Wissman AM, Farin FM, Bammler TK, Beyer RP, Clayton DF, Perkel DJ, Brenowitz EA (2012) Seasonal changes in patterns of gene expression in avian song control brain regions. PLoS One 7:e35119. CrossRef Medline
40. Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23:251-258. CrossRef Medline
41. Tramontin AD, Smith GT, Breuner CW, Brenowitz EA (1998) Seasonal plasticity and sexual dimorphism in the avian song control system: stereological measurement of neuron density and number. J Comp Neurol 396:186 -192. CrossRef Medline
42. Tramontin AD, Hartman VN, Brenowitz EA (2000) Breeding conditions induce rapid and sequential growth in adult avian song control circuits: a model of seasonal plasticity in the brain. J Neurosci 20:854-861. Medline
43. Walton C, Pariser E, Nottebohm F (2012) The zebra finch paradox: song is little changed, but number of neurons doubles. J Neurosci 32:761-774. CrossRef Medline
44. Wang N, Hurley P, Pytte C, Kirn JR (2002) Vocal control neuron incorporation decreases with age in the adult zebra finch. J Neurosci 22:10864- 10870. Medline
45. Wiltrout C, Lang B, Yan Y, Dempsey RJ, Vemuganti R (2007) Repairing brain after stroke: a review on post-ischemic neurogenesis. Neurochem Int 50:1028 -1041. CrossRef Medline
46. Wissman AM, Brenowitz EA (2009) The role of neurotrophins in the seasonal-like growth of the avian song control system. J Neurosci 29: 6461-6471. CrossRef Medline
47. Zupanc GK (2009) Towards brain repair: insights from teleost fish. Semin Cell Dev Biol 20:683- 690. CrossRef Medline