Adult-born neurons modify excitatory synaptic transmission to existing neurons

eLife

Volumn 6, Issue , 2017, Pages

  Adlaf, Elena W ^a   Vaden, Ryan J ^a   Niver, Anastasia J ^a   Manuel, Allison F ^a   Onyilo, Vincent C ^a   Araujo, Matheus T ^a   Dieni, Cristina V ^a   Vo, Hai T ^a   King, Gwendalyn D ^a   Wadiche, Jacques I ^a   Overstreet Wadiche, Linda ^a  

^a University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PICROTOXIN; PROTEIN BAX; VESICULAR GLUTAMATE TRANSPORTER;

ABLATION THERAPY; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL DENSITY; CELL MATURATION; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; EXCITATORY SYNAPTIC TRANSMISSION; GENE DELETION; GRANULE CELL; IMMATURITY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; STEREOLOGY; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; NERVE CELL NETWORK; PHYSIOLOGY;

ANIMALS; DENTATE GYRUS; EXCITATORY POSTSYNAPTIC POTENTIALS; MICE; NERVE NET; NEUROGENESIS; NEURONS; SYNAPTIC TRANSMISSION;

EID: 85011332604     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.19886     Document Type: Article

References (82)

1. Aimone JB, Deng W, Gage FH. 2011. Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70:589–596. doi: 10.1016/j.neuron.2011.05.010
2. Akers KG, Martinez-Canabal A, Restivo L, Yiu AP, De Cristofaro A, Hsiang HL, Wheeler AL, Guskjolen A, Niibori Y, Shoji H, Ohira K, Richards BA, Miyakawa T, Josselyn SA, Frankland PW. 2014. Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 344:598–602. doi: 10.1126/science.1248903
3. Ambrogini P, Cuppini R, Lattanzi D, Ciuffoli S, Frontini A, Fanelli M. 2010. Synaptogenesis in adult-generated hippocampal granule cells is affected by behavioral experiences. Hippocampus 20:799–810. doi: 10.1002/hipo. 20679
4. Arruda-Carvalho M, Sakaguchi M, Akers KG, Josselyn SA, Frankland PW. 2011. Posttraining ablation of adult-generated neurons degrades previously acquired memories. Journal of Neuroscience 31:15113–15127. doi: 10. 1523/JNEUROSCI.3432-11.2011
5. Bekkers JM, Clements JD. 1999. Quantal amplitude and quantal variance of strontium-induced asynchronous EPSCs in rat dentate granule neurons. The Journal of Physiology 516:227–248. doi: 10.1111/j.1469-7793.1999. 227aa.x
6. Bergami M, Masserdotti G, Temprana SG, Motori E, Eriksson TM, Göbel J, Yang SM, Conzelmann KK, Schinder AF, Götz M, Berninger B. 2015. A critical period for experience-dependent remodeling of adult-born neuron connectivity. Neuron 85:710–717. doi: 10.1016/j.neuron.2015.01.001
7. Bosch C, Martínez A, Masachs N, Teixeira CM, Fernaud I, Ulloa F, Pérez-Martínez E, Lois C, Comella JX, DeFelipe J, Merchán-Pérez A, Soriano E. 2015. FIB/SEM technology and high-throughput 3D reconstruction of dendritic spines and synapses in GFP-labeled adult-generated neurons. Frontiers in Neuroanatomy 9:60. doi: 10.3389/ fnana.2015.00060
8. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, Kuhn HG, Praag, h VAN, Kuhn HG. 2003. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. European Journal of Neuroscience 17:2042–2046. doi: 10.1046/j.1460-9568.2003.02647.x
9. Brunner J, Neubrandt M, Van-Weert S, Andrási T, Kleine Borgmann FB, Jessberger S, Szabadics J. 2014. Adult-born granule cells mature through two functionally distinct states. eLife 3:e03104. doi: 10.7554/eLife.03104
10. Buch T, Heppner FL, Tertilt C, Heinen TJ, Kremer M, Wunderlich FT, Jung S, Waisman A. 2005. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nature Methods 2:419–426. doi: 10.1038/nmeth762
11. Chambers RA, Potenza MN, Hoffman RE, Miranker W. 2004. Simulated apoptosis/neurogenesis regulates learning and memory capabilities of adaptive neural networks. Neuropsychopharmacology 29:747–758. doi: 10. 1038/sj.npp.1300358
12. Chancey JH, Adlaf EW, Sapp MC, Pugh PC, Wadiche JI, Overstreet-Wadiche LS. 2013. GABA depolarization is required for experience-dependent synapse unsilencing in adult-born neurons. Journal of Neuroscience 33: 6614–6622. doi: 10.1523/JNEUROSCI.0781-13.2013
13. Dieni CV, Nietz AK, Panichi R, Wadiche JI, Overstreet-Wadiche L. 2013. Distinct determinants of sparse activation during granule cell maturation. Journal of Neuroscience 33:19131–19142. doi: 10.1523/JNEUROSCI. 2289-13.2013
14. Dieni CV, Panichi R, Aimone JB, Kuo CT, Wadiche JI, Overstreet-Wadiche L. 2016. Low excitatory innervation balances high intrinsic excitability of immature dentate neurons. Nature Communications 7:11313. doi: 10. 1038/ncomms11313
15. Drew LJ, Kheirbek MA, Luna VM, Denny CA, Cloidt MA, Wu MV, Jain S, Scharfman HE, Hen R. 2016. Activation of local inhibitory circuits in the dentate gyrus by adult-born neurons. Hippocampus 26:763–778. doi: 10.1002/ hipo.22557
16. Eadie BD, Redila VA, Christie BR. 2005. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. The Journal of Comparative Neurology 486:39–47. doi: 10.1002/cne.20493
17. Enikolopov G, Overstreet-Wadiche L, Ge S. 2015. Viral and transgenic reporters and genetic analysis of adult neurogenesis. Cold Spring Harbor Perspectives in Biology 7:a018804. doi: 10.1101/cshperspect.a018804
18. Epp JR, Silva Mera R, Köhler S, Josselyn SA, Frankland PW. 2016. Neurogenesis-mediated forgetting minimizes proactive interference. Nature Communications 7:10838. doi: 10.1038/ncomms10838
19. Ertürk A, Wang Y, Sheng M. 2014. Local pruning of dendrites and spines by caspase-3-dependent and proteasome-limited mechanisms. Journal of Neuroscience 34:1672–1688. doi: 10.1523/JNEUROSCI.3121-13. 2014
20. Espósito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF. 2005. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. Journal of Neuroscience 25: 10074–10086. doi: 10.1523/JNEUROSCI.3114-05.2005
21. Foster TC, Dumas TC. 2001. Mechanism for increased hippocampal synaptic strength following differential experience. Journal of Neurophysiology 85:1377–1383.
22. Foster TC, Gagne J, Massicotte G. 1996. Mechanism of altered synaptic strength due to experience: relation to long-term potentiation. Brain Research 736:243–250. doi: 10.1016/0006-8993(96)00707-X
23. Gao X, Arlotta P, Macklis JD, Chen J. 2007. Conditional knock-out of beta-catenin in postnatal-born dentate gyrus granule neurons results in dendritic malformation. Journal of Neuroscience 27:14317–14325. doi: 10. 1523/JNEUROSCI.3206-07.2007
24. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589–593. doi: 10.1038/nature04404
25. Ge S, Yang CH, Hsu KS, Ming GL, Song H. 2007. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559–566. doi: 10.1016/j.neuron.2007.05.002
26. Gil-Mohapel J, Brocardo PS, Choquette W, Gothard R, Simpson JM, Christie BR. 2013. Hippocampal neurogenesis levels predict WATERMAZE search strategies in the aging brain. PLoS One 8:e75125. doi: 10.1371/journal.pone.0075125
27. Green EJ, Greenough WT. 1986. Altered synaptic transmission in Dentate Gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro. Journal of Neurophysiology 55:739–750
28. Hill AS, Sahay A, Hen R. 2015. Increasing adult hippocampal neurogenesis is sufficient to reduce anxiety and Depression-Like behaviors. Neuropsychopharmacology 40:2368–2378. doi: 10.1038/npp.2015.85
29. Ikrar T, Guo N, He K, Besnard A, Levinson S, Hill A, Lee HK, Hen R, Xu X, Sahay A. 2013. Adult neurogenesis modifies excitability of the dentate gyrus. Frontiers in Neural Circuits 7:204. doi: 10.3389/fncir.2013.00204
30. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R. 2008. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nature Neuroscience 11:1153–1161. doi: 10.1038/nn.2185
31. Jiao S, Li Z. 2011. Nonapoptotic function of BAD and BAX in long-term depression of synaptic transmission. Neuron 70:758–772. doi: 10.1016/j.neuron.2011.04.004
32. Jung CK, Herms J. 2014. Structural dynamics of dendritic spines are influenced by an environmental enrichment: an in vivo imaging study. Cerebral Cortex 24:377–384. doi: 10.1093/cercor/bhs317
33. Kajimoto K, Valenzuela CF, Allan AM, Ge S, Gu Y, Cunningham LA. 2016. Prenatal alcohol exposure alters synaptic activity of adult hippocampal dentate granule cells under conditions of enriched environment. Hippocampus 26:1078–1087. doi: 10.1002/hipo.22588
34. Kavalali ET. 2015. The mechanisms and functions of spontaneous neurotransmitter release. Nature Reviews Neuroscience 16:5–16. doi: 10.1038/nrn3875
35. Kim WR, Park OH, Choi S, Choi SY, Park SK, Lee KJ, Rhyu IJ, Kim H, Lee YK, Kim HT, Oppenheim RW, Sun W. 2009. The maintenance of specific aspects of neuronal function and behavior is dependent on programmed cell death of adult-generated neurons in the dentate gyrus. European Journal of Neuroscience 29:1408–1421. doi: 10.1111/j.1460-9568.2009.06693.x
36. Kuo CT, Mirzadeh Z, Soriano-Navarro M, Rasin M, Wang D, Shen J, Sestan N, Garcia-Verdugo J, Alvarez-Buylla A, Jan LY, Jan YN. 2006a. Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 127:1253–1264. doi: 10.1016/j.cell.2006.10.041
37. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN. 2006b. Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51:283–290. doi: 10.1016/j.neuron. 2006.07.014
38. Lagace DC, Whitman MC, Noonan MA, Ables JL, DeCarolis NA, Arguello AA, Donovan MH, Fischer SJ, Farnbauch LA, Beech RD, DiLeone RJ, Greer CA, Mandyam CD, Eisch AJ. 2007. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. Journal of Neuroscience 27:12623–12629. doi: 10.1523/ JNEUROSCI.3812-07.2007
39. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, et al. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176. doi: 10.1038/ nature05453
40. Li Z, Jo J, Jia JM, Lo SC, Whitcomb DJ, Jiao S, Cho K, Sheng M. 2010. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141:859–871. doi: 10.1016/j.cell. 2010.03.053
41. Lo SC, Wang Y, Weber M, Larson JL, Scearce-Levie K, Sheng M. 2015. Caspase-3 deficiency results in disrupted synaptic homeostasis and impaired attention control. Journal of Neuroscience 35:2118–2132. doi: 10.1523/ JNEUROSCI.3280-14.2015
42. Malik R, Chattarji S. 2012. Enhanced intrinsic excitability and EPSP-spike coupling accompany enriched environment-induced facilitation of LTP in hippocampal CA1 pyramidal neurons. Journal of Neurophysiology 107:1366–1378. doi: 10.1152/jn.01009.2011
43. Marín-Burgin A, Mongiat LA, Pardi MB, Schinder AF. 2012. Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 335:1238–1242. doi: 10.1126/science.1214956
44. Massa F, Koehl M, Koelh M, Wiesner T, Grosjean N, Revest JM, Piazza PV, Abrous DN, Oliet SH. 2011. Conditional reduction of adult neurogenesis impairs bidirectional hippocampal synaptic plasticity. PNAS 108: 6644–6649. doi: 10.1073/pnas.1016928108
45. McAvoy KM, Scobie KN, Berger S, Russo C, Guo N, Decharatanachart P, Vega-Ramirez H, Miake-Lye S, Whalen M, Nelson M, Bergami M, Bartsch D, Hen R, Berninger B, Sahay A. 2016. Modulating neuronal competition dynamics in the dentate gyrus to rejuvenate aging memory circuits. Neuron 91:1356–1373. doi: 10.1016/j. neuron.2016.08.009
46. Mongiat LA, Espósito MS, Lombardi G, Schinder AF. 2009. Reliable activation of immature neurons in the adult hippocampus. PLoS One 4:e5320. doi: 10.1371/journal.pone.0005320
47. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S, Rodriguez B, V, Tonegawa S. 2012. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188– 201. doi: 10.1016/j.cell.2012.01.046
48. Oh WC, Hill TC, Zito K. 2013. Synapse-specific and size-dependent mechanisms of spine structural plasticity accompanying synaptic weakening. PNAS 110:E305–E312. doi: 10.1073/pnas.1214705110
49. Olson AK, Eadie BD, Ernst C, Christie BR. 2006. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16:250–260. doi: 10.1002/hipo.20157
50. Overstreet LS, Hentges ST, Bumaschny VF, de Souza FS, Smart JL, Santangelo AM, Low MJ, Westbrook GL, Rubinstein M, Souza, f DE, Rubinstein M. 2004. A transgenic marker for newly born granule cells in Dentate Gyrus. Journal of Neuroscience 24:3251–3259. doi: 10.1523/JNEUROSCI.5173-03.2004
51. Overstreet-Wadiche LS, Bensen AL, Westbrook GL. 2006. Delayed development of adult-generated granule cells in Dentate Gyrus. Journal of Neuroscience 26:2326–2334. doi: 10.1523/JNEUROSCI.4111-05.2006
52. Overstreet-Wadiche LS, Westbrook GL. 2006. Functional maturation of adult-generated granule cells. Hippocampus 16:208–215. doi: 10.1002/hipo.20152
53. Petersen RP, Moradpour F, Eadie BD, Shin JD, Kannangara TS, Delaney KR, Christie BR. 2013. Electrophysiological identification of medial and lateral perforant path inputs to the dentate gyrus. Neuroscience 252:154–168. doi: 10.1016/j.neuroscience.2013.07.063
54. Pugh P, Adlaf E, Zhao CS, Markwardt S, Gavin C, Wadiche J, Overstreet-Wadiche L. 2011. Enhanced integration of newborn neurons after neonatal insults. Frontiers in Neuroscience 5:45. doi: 10.3389/fnins.2011.00045
55. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ. 2000. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nature Neuroscience 3:238– 244. doi: 10.1038/72945
56. Riccomagno MM, Kolodkin AL. 2015. Sculpting neural circuits by axon and dendrite pruning. Annual Review of Cell and Developmental Biology 31:779–805. doi: 10.1146/annurev-cellbio-100913-013038
57. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL. 2008. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 3:e1997 doi: 10. 1371/journal.pone.0001997
58. Rudolph S, Overstreet-Wadiche L, Wadiche JI. 2011. Desynchronization of multivesicular release enhances purkinje cell output. Neuron 70:991–1004. doi: 10.1016/j.neuron.2011.03.029
59. Sahay A, Scobie KN, Hill AS, O’Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R. 2011. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466–470. doi: 10.1038/nature09817
60. Schmidt-Hieber C, Jonas P, Bischofberger J. 2004. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184–187. doi: 10.1038/nature02553
61. Sheng M, Ertürk A. 2014. Long-term depression: a cell biological view. Philosophical Transactions of the Royal Society B: Biological Sciences 369:20130138. doi: 10.1098/rstb.2013.0138
62. Shipton OA, Paulsen O. 2014. GluN2A and GluN2B subunit-containing NMDA receptors in hippocampal plasticity. Philosophical Transactions of the Royal Society B: Biological Sciences 369:20130163. doi: 10.1098/ rstb.2013.0163
63. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M. 2010. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483–495. doi: 10.1016/j.stem.2010.08.014
64. Singer BH, Gamelli AE, Fuller CL, Temme SJ, Parent JM, Murphy GG. 2011. Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice. PNAS 108:5437–5442. doi: 10.1073/pnas.1015425108
65. Stranahan AM, Khalil D, Gould E. 2007. Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus 17:1017–1022. doi: 10.1002/hipo.20348
66. Sun W, Winseck A, Vinsant S, Park OH, Kim H, Oppenheim RW. 2004. Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene bax. Journal of Neuroscience 24: 11205–11213. doi: 10.1523/JNEUROSCI.1436-04.2004
67. Swanger SA, Yao X, Gross C, Bassell GJ. 2011. Automated 4D analysis of dendritic spine morphology: applications to stimulus-induced spine remodeling and pharmacological rescue in a disease model. Molecular Brain 4:38. doi: 10.1186/1756-6606-4-38
68. Tashiro A, Makino H, Gage FH. 2007. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. Journal of Neuroscience 27:3252–3259. doi: 10. 1523/JNEUROSCI.4941-06.2007
69. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH. 2006. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442:929–933. doi: 10.1038/nature05028
70. Temprana SG, Mongiat LA, Yang SM, Trinchero MF, Alvarez DD, Kropff E, Giacomini D, Beltramone N, Lanuza GM, Schinder AF. 2015. Delayed coupling to feedback inhibition during a critical period for the integration of adult-born granule cells. Neuron 85:116–130. doi: 10.1016/j.neuron.2014.11.023
71. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF. 2008. Neurons born in the adult dentate gyrus form functional synapses with target cells. Nature Neuroscience 11:901–907. doi: 10.1038/nn. 2156
72. Toni N, Sultan S. 2011. Synapse formation on adult-born hippocampal neurons. European Journal of Neuroscience 33:1062–1068. doi: 10.1111/j.1460-9568.2011.07604.x
73. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH. 2007. Synapse formation on neurons born in the adult hippocampus. Nature Neuroscience 10:727–734. doi: 10.1038/nn1908
74. Unsain N, Barker PA. 2015. New views on the misconstrued: Executioner caspases and their diverse Nonapoptotic roles. Neuron 88:461–474. doi: 10.1016/j.neuron.2015.08.029
75. van Praag H, Kempermann G, Gage FH. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience 2:266–270. doi: 10.1038/6368
76. Vukovic J, Borlikova GG, Ruitenberg MJ, Robinson GJ, Sullivan RK, Walker TL, Bartlett PF. 2013. Immature doublecortin-positive hippocampal neurons are important for learning but not for remembering. Journal of Neuroscience 33:6603–6613. doi: 10.1523/JNEUROSCI.3064-12.2013
77. Weisz VI, Argibay PF. 2012. Neurogenesis interferes with the retrieval of remote memories: forgetting in neurocomputational terms. Cognition 125:13–25. doi: 10.1016/j.cognition.2012.07.002
78. Wiegert JS, Oertner TG. 2013. Long-term depression triggers the selective elimination of weakly integrated synapses. PNAS 110:E4510–E4519. doi: 10.1073/pnas.1315926110
79. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW. 2006. Local caspase activity directs engulfment of dendrites during pruning. Nature Neuroscience 9:1234–1236. doi: 10.1038/nn1774
80. Williams MR, DeSpenza T, Li M, Gulledge AT, Luikart BW. 2015. Hyperactivity of newborn Pten knock-out neurons results from increased excitatory synaptic drive. Journal of Neuroscience 35:943–959. doi: 10.1523/ JNEUROSCI.3144-14.2015
81. Wu G, Malinow R, Cline HT. 1996. Maturation of a central glutamatergic synapse. Science 274:972–976. doi: 10. 1126/science.274.5289.972
82. Yun S, Donovan MH, Ross MN, Richardson DR, Reister R, Farnbauch LA, Fischer SJ, Riethmacher D, Gershenfeld HK, Lagace DC, Eisch AJ. 2016. Stress-Induced Anxiety- and Depressive-like Phenotype associated with transient reduction in Neurogenesis in adult Nestin-CreERT2/Diphtheria Toxin fragment A transgenic mice. PLoS One 11:e0147256. doi: 10.1371/journal.pone.0147256