Prenatal alcohol exposure alters synaptic activity of adult hippocampal dentate granule cells under conditions of enriched environment

Hippocampus

Volumn 26, Issue 8, 2016, Pages 1078-1087

  Kajimoto, Kenta ^a   Valenzuela, C Fernando ^a   Allan, Andrea M ^a   Ge, Shaoyu ^a,b   Gu, Yan ^a,b   Cunningham, Lee Anna ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b Stony Brook University   (United States)

Author keywords

electrophysiology; environmental enrichment; fetal alcohol spectrum disorder; neurogenesis

Indexed keywords

ALCOHOL;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS GRANULAR LAYER; ELECTROPHYSIOLOGICAL PROCEDURES; EMBRYO DEVELOPMENT; FEMALE; MALE; MOUSE; NERVE EXCITABILITY; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP;

EID: 84978861862     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22588     Document Type: Article

References (45)

1. Allan AM, Wu H, Paxton LL, Savage DD. 1998. Prenatal ethanol exposure alters the modulation of the gamma-aminobutyric acidA1 receptor-gated chloride ion channel in adult rat offspring. J Pharmacol Exp Therap 284:250–257.
2. Bergami M, Masserdotti G, Temprana SG, Motori E, Eriksson TM, Gobel J, Yang SM, Conzelmann KK, Schinder AF, Gotz M, et al. 2015. A critical period for experience-dependent remodeling of adult-born neuron connectivity. Neuron 85:710–717.
3. Berman RF, Hannigan JH. 2000. Effects of prenatal alcohol exposure on the hippocampus: Spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10:94–110.
4. Boehme F, Gil-Mohapel J, Cox A, Patten A, Giles E, Brocardo PS, Christie BR. 2011. Voluntary exercise induces adult hippocampal neurogenesis and BDNF expression in a rodent model of fetal alcohol spectrum disorders. Eur J Neurosci 33:1799–1811.
5. Brady ML, Allan AM, Caldwell KK. 2012. A limited access mouse model of prenatal alcohol exposure that produces long-lasting deficits in hippocampal-dependent learning and memory. Alcoholism Clin Exp Res 36:457–466.
6. Brady ML, Diaz MR, Iuso A, Everett JC, Valenzuela CF, Caldwell KK. 2013. Moderate prenatal alcohol exposure reduces plasticity and alters NMDA receptor subunit composition in the dentate gyrus. J NeuroscOff J Soc Neurosci 33:1062–1067.
7. Choi IY, Allan AM, Cunningham LA. 2005. Moderate fetal alcohol exposure impairs the neurogenic response to an enriched environment in adult mice. Alcohol Clin Exp Res 29:2053–2062.
8. Diaz MR, Jotty K, Locke JL, Jones SR, Valenzuela CF. 2014. Moderate alcohol exposure during the rat equivalent to the third trimester of human pregnancy alters regulation of GABAA receptor-mediated synaptic transmission by dopamine in the basolateral amygdala. Front Pediatr 2:46.
9. Eckert MJ, Abraham WC. 2013. Effects of environmental enrichment exposure on synaptic transmission and plasticity in the hippocampus. Curr Top Behav Neurosci 15:165–187.
10. 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.
11. 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.
12. Gil-Mohapel J, Boehme F, Kainer L, Christie BR. 2010. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: Insights from different rodent models. Brain Res Rev 64:283–303.
13. Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, Frankland PW, Ge S. 2012. Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 15:1700–1706.
14. Helfer JL, Calizo LH, Dong WK, Goodlett CR, Greenough WT, Klintsova AY. 2009. Binge-like postnatal alcohol exposure triggers cortical gliogenesis in adolescent rats. J Comp Neurol 514:259–271.
15. Ieraci A, Herrera DG. 2007. Single alcohol exposure in early life damages hippocampal stem/progenitor cells and reduces adult neurogenesis. Neurobiol Dis 26:597–605.
16. Kajimoto K, Allan A, Cunningham LA. 2013. Fate analysis of adult hippocampal progenitors in a murine model of fetal alcohol spectrum disorder (FASD). PLoS One 8:e73788.
17. Kheirbek MA, Tannenholz L, Hen R. 2012. NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J Neurosci Off J Soc Neurosci 32:8696–8702.
18. Kim WR, Christian K, Ming GL, Song H. 2012. Time-dependent involvement of adult-born dentate granule cells in behavior. Behav Brain Res 227:470–479.
19. Klintsova AY, Helfer JL, Calizo LH, Dong WK, Goodlett CR, Greenough WT. 2007. Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcoholism Clin Exp Res 31:2073–2082.
20. Kodituwakku PW, Kodituwakku EL. 2011. From research to practice: An integrative framework for the development of interventions for children with fetal alcohol spectrum disorders. Neuropsychol Rev 21:204–223.
21. Koike-Tani M, Saitoh N, Takahashi T. 2005. Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J Neurosci Off J Soc Neurosci 25:199–207.
22. Laplagne DA, Esposito MS, Piatti VC, Morgenstern NA, Zhao C, van Praag H, Gage FH, Schinder AF. 2006. Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4:e409.
23. Lemaire V, Tronel S, Montaron MF, Fabre A, Dugast E, Abrous DN. 2012. Long-lasting plasticity of hippocampal adult-born neurons. J Neurosci Off J Soc Neurosci 32:3101–3108.
24. Malik R, Chattarji S. 2012. Enhanced intrinsic excitability and EPSP-spike coupling accompany enriched environment-induced facilitation of LTP in hippocampal CA1 pyramidal neurons. J Neurophysiol 107:1366–1378.
25. Mathews EA, Morgenstern NA, Piatti VC, Zhao C, Jessberger S, Schinder AF, Gage FH. 2010. A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis. J Comp Neurol 518:4479–4490.
26. Mattson SN, Crocker N, Nguyen TT. 2011. Fetal alcohol spectrum disorders: Neuropsychological and behavioral features. Neuropsychol Rev 21:81–101.
27. May PA, Gossage JP, Kalberg WO, Robinson LK, Buckley D, Manning M, Hoyme HE. 2009. Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies. Dev Disabil Res Rev 15:176–192.
28. Muramatsu R, Ikegaya Y, Matsuki N, Koyama R. 2007. Neonatally born granule cells numerically dominate adult mice dentate gyrus. Neuroscience 148:593–598.
29. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, et al. 2012. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188–201.
30. Parsley SL, Pilgram SM, Soto F, Giese KP, Edwards FA. 2007. Enriching the environment of alphaCaMKIIT286A mutant mice reveals that LTD occurs in memory processing but must be subsequently reversed by LTP. Learn Mem 14:75–83.
31. Piatti VC, Davies-Sala MG, Esposito MS, Mongiat LA, Trinchero MF, Schinder AF. 2011. The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci Off J Soc Neurosci 31:7715–7728.
32. Piatti VC, Ewell LA, Leutgeb JK. 2013. Neurogenesis in the dentate gyrus: Carrying the message or dictating the tone. Front Neurosci 7:50.
33. Redila VA, Olson AK, Swann SE, Mohades G, Webber AJ, Weinberg J, Christie BR. 2006. Hippocampal cell proliferation is reduced following prenatal ethanol exposure but can be rescued with voluntary exercise. Hippocampus 16:305–311.
34. Riley EP, Infante MA, Warren KR. 2011. Fetal alcohol spectrum disorders: An overview. Neuropsychol Rev 21:73–80.
35. Rouach N, Byrd K, Petralia RS, Elias GM, Adesnik H, Tomita S, Karimzadegan S, Kealey C, Bredt DS, Nicoll RA. 2005. TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity. Nat Neurosci 8:1525–1533.
36. Samudio-Ruiz SL, Allan AM, Sheema S, Caldwell KK. 2010. Hippocampal N-methyl-d-aspartate receptor subunit expression profiles in a mouse model of prenatal alcohol exposure. Alcoholism Clin Exp Res 34:342–353.
37. Savage DD, Queen SA, Sanchez CF, Paxton LL, Mahoney JC, Goodlett CR, West JR. 1992. Prenatal ethanol exposure during the last third of gestation in rat reduces hippocampal NMDA agonist binding site density in 45-day-old offspring. Alcohol 9:37–41.
38. Sommer B, Keinanen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Kohler M, Takagi T, Sakmann B, Seeburg PH. 1990. Flip and flop: A cell-specific functional switch in glutamate-operated channels of the CNS. Science 249:1580–1585.
39. Sutherland RJ, McDonald RJ, Savage DD. 1997. Prenatal exposure to moderate levels of ethanol can have long-lasting effects on hippocampal synaptic plasticity in adult offspring. Hippocampus 7:232–238.
40. Tronel S, Fabre A, Charrier V, Oliet SH, Gage FH, Abrous DN. 2010. Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc Natl Acad Sci USA 107:7963–7968.
41. Valenzuela CF, Morton RA, Diaz MR, Topper L. 2012. Does moderate drinking harm the fetal brain? Insights from animal models. Trends Neurosci 35:284–292.
42. Varaschin RK, Akers KG, Rosenberg MJ, Hamilton DA, Savage DD. 2010. Effects of the cognition-enhancing agent ABT-239 on fetal ethanol-induced deficits in dentate gyrus synaptic plasticity. J Pharmacol Exp Therap 334:191–198.
43. Vivar C, Peterson BD, van Praag H. 2015. Running rewires the neuronal network of adult-born dentate granule cells. NeuroImage.
44. Zhao C, Jou J, Wolff LJ, Sun H, Gage FH. 2015. Spine morphogenesis in newborn granule cells is differentially regulated in the outer and middle molecular layers. J Comp Neurol 523:1588.
45. Zhao C, Teng EM, Summers RG Jr., Ming GL, Gage FH. 2006. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci Off J Soc Neurosci 26:3–11.