Synaptic pruning in the female hippocampus is triggered at puberty by extrasynaptic GABAA receptors on dendritic spines

eLife

Volumn 5, Issue MAY2016, 2016, Pages

  Afroz, Sonia ^a,b,d   Parato, Julie ^a,b   Shen, Hui ^a,c   Smith, Sheryl Sue ^a  

^a Downstate Health Sciences University   (United States)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4; KALIRIN 7; MEMANTINE; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

ACTIVE AVOIDANCE TEST; ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; COGNITIVE DEVELOPMENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC SPINE; EXCITATORY POSTSYNAPTIC POTENTIAL; EXPERIMENTAL COGNITIVE TEST; FEMALE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; MULTIPLE PLACEMENT OBJECT RECOGNITION TEST; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; PUBERTY; SPATIAL LEARNING; SYNAPTIC PRUNING; TASK PERFORMANCE; ANIMAL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PYRAMIDAL NERVE CELL;

ANIMALS; DENDRITIC SPINES; FEMALE; HIPPOCAMPUS; MICE; NEURONAL PLASTICITY; PUBERTY; PYRAMIDAL CELLS; RECEPTORS, GABA-A;

EID: 84971635823     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15106     Document Type: Article

References (85)

1. Alvarez VA, Ridenour DA, Sabatini BL. 2007. Distinct structural and ionotropic roles of NMDA receptors in controlling spine and synapse stability. Journal of Neuroscience 27:7365–7376. doi: 10.1523/JNEUROSCI.0956-07.2007.
2. Aoki C, Sabaliauskas N, Chowdhury T, Min JY, Colacino AR, Laurino K, Barbarich-Marsteller NC. 2012. Adolescent female rats exhibiting activity-based anorexia express elevated levels of GABA(A) receptor a4 and d subunits at the plasma membrane of hippocampal CA1 spines. Synapse 66:391–407. doi: 10.1002/syn.21528.
3. Arellano JI, Benavides-Piccione R, Defelipe J, Yuste R. 2007. Ultrastructure of dendritic spines: Correlation between synaptic and spine morphologies. Frontiers in Neuroscience 1:131–143. doi: 10.3389/neuro.01.1.1.010.2007.
4. Bannerman DM, Niewoehner B, Lyon L, Romberg C, Schmitt WB, Taylor A, Sanderson DJ, Cottam J, Sprengel R, Seeburg PH, Köhr G, Rawlins JN, Köhr G, Rawlins JN. 2008. NMDA receptor subunit NR2A is required for rapidly acquired spatial working memory but not incremental spatial reference memory. Journal of Neuroscience 28:3623–3630. doi: 10.1523/JNEUROSCI.3639-07.2008.
5. Barker GR, Warburton EC. 2011. When is the hippocampus involved in recognition memory? Journal of Neuroscience 31:10721–10731. doi: 10.1523/JNEUROSCI.6413-10.2011.
6. Bell ME, Bourne JN, Chirillo MA, Mendenhall JM, Kuwajima M, Harris KM. 2014. Dynamics of nascent and active zone ultrastructure as synapses enlarge during long-term potentiation in mature hippocampus. The Journal of Comparative Neurology 522:3861–3884. doi: 10.1002/cne.23646.
7. Beltrán-Campos V, Prado-Alcalá RA, León-Jacinto U, Aguilar-Vázquez A, Quirarte GL, Ramírez-Amaya V, Díaz- Cintra S. 2011. Increase of mushroom spine density in CA1 apical dendrites produced by water maze training is prevented by ovariectomy. Brain Research 1369:119–130. doi: 10.1016/j.brainres.2010.10.105.
8. Bourne J, Harris KM. 2007. Do thin spines learn to be mushroom spines that remember? Current Opinion in Neurobiology 17:381–386. doi: 10.1016/j.conb.2007.04.009.
9. Brown N, Kerby J, Bonnert TP, Whiting PJ, Wafford KA. 2002. Pharmacological characterization of a novel cell line expressing human alpha(4)beta(3)delta GABA(A) receptors. British Journal of Pharmacology 136:965–974. doi: 10.1038/sj.bjp.0704795.
10. Bullock WM, Cardon K, Bustillo J, Roberts RC, Perrone-Bizzozero NI. 2008. Altered expression of genes involved in gabaergic transmission and neuromodulation of granule cell activity in the cerebellum of schizophrenia patients. The American Journal of Psychiatry 165:1594–1603. doi: 10.1176/appi.ajp.2008.07121845.
11. Campbell IG, Grimm KJ, de Bie E, Feinberg I. 2012. Sex, puberty, and the timing of sleep EEG measured adolescent brain maturation. Proceedings of the National Academy of Sciences of the United States of America 109:5740–5743. doi: 10.1073/pnas.1120860109.
12. Caraiscos VB, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, Orser BA. 2004. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors. Proceedings of the National Academy of Sciences of the United States of America 101:3662–3667. doi: 10.1073/pnas.0307231101.
13. Chandra D, Jia F, Liang J, Peng Z, Suryanarayanan A, Werner DF, Spigelman I, Houser CR, Olsen RW, Harrison NL, Homanics GE. 2006. GABAA receptor alpha 4 subunits mediate extrasynaptic inhibition in thalamus and dentate gyrus and the action of gaboxadol. Proceedings of the National Academy of Sciences of the United States of America 103:15230–15235. doi: 10.1073/pnas.0604304103.
14. Chechik G, Meilijson I, Ruppin E. 1999. Neuronal regulation: A biologically plausible mechanism for efficient synaptic pruning in development. Neurocomputing 26-27:633–639. doi: 10.1016/S0925-2312(98)00161-1.
15. Chen Y, Liang Z, Fei E, Chen Y, Zhou X, Fang W, Fu WY, Fu AK, Ip NY. 2015. Axin regulates dendritic spine morphogenesis through cdc42-dependent signaling. PloS One 10:e0133115. doi: 10.1371/journal.pone.0133115.
16. Cole PD, Vijayanathan V, Ali NF, Wagshul ME, Tanenbaum EJ, Price J, Dalal V, Gulinello ME. 2013. Memantine protects rats treated with intrathecal methotrexate from developing spatial memory deficits. Clinical Cancer Research 19:4446–4454. doi: 10.1158/1078-0432.CCR-13-1179.
17. Collins AL, Ma D, Whitehead PL, Martin ER, Wright HH, Abramson RK, Hussman JP, Haines JL, Cuccaro ML, Gilbert JR, Pericak-Vance MA. 2006. Investigation of autism and GABA receptor subunit genes in multiple ethnic groups. Neurogenetics 7:167–174. doi: 10.1007/s10048-006-0045-1.
18. Croen LA, Grether JK, Selvin S. 2002. Descriptive epidemiology of autism in a california population: Who is at risk? Journal of Autism and Developmental Disorders 32:217–224. doi: 10.1023/A:1015405914950.
19. D’Cruz AM, Ragozzino ME, Mosconi MW, Shrestha S, Cook EH, Sweeney JA. 2013. Reduced behavioral flexibility in autism spectrum disorders. Neuropsychology 27:152–160. doi: 10.1037/a0031721.
20. Dumitriu D, Hao J, Hara Y, Kaufmann J, Janssen WG, Lou W, Rapp PR, Morrison JH. 2010. Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. Journal of Neuroscience 30:7507–7515. doi: 10.1523/JNEUROSCI.6410-09.2010.
21. Dunwiddie T, Lynch G. 1978. Long-term potentiation and depression of synaptic responses in the rat hippocampus: Localization and frequency dependency. The Journal of Physiology 276:353–367. doi: 10.1113/jphysiol.1978.sp012239.
22. Fatemi SH, Reutiman TJ, Folsom TD, Rooney RJ, Patel DH, Thuras PD. 2010. mRNA and protein levels for gabaaalpha4, alpha5, beta1 and GABABR1 receptors are altered in brains from subjects with autism. Journal of Autism and Developmental Disorders 40:743–750. doi: 10.1007/s10803-009-0924-z
23. Friedman SB, Ader R, Grota LJ, Larson T. 1967. Plasma corticosterone response to parameters of electric shock stimulation in the rat. Psychosomatic Medicine 29:323–328. doi: 10.1097/00006842-196707000-00003.
24. Gao C, Frausto SF, Guedea AL, Tronson NC, Jovasevic V, Leaderbrand K, Corcoran KA, Guzmán YF, Swanson GT, Radulovic J. 2011. IQGAP1 regulates NR2A signaling, spine density, and cognitive processes. Journal of Neuroscience 31:8533–8542. doi: 10.1523/JNEUROSCI.1300-11.2011.
25. Gao XM, Tamminga CA. 1995. MK801 induces late regional increases in NMDA and kainate receptor binding in rat brain. Journal of Neural Transmission. General Section 101:105–113. doi: 10.1007/BF01271549.
26. Gillberg C, Steffenburg S. 1987. Outcome and prognostic factors in infantile autism and similar conditions: A population-based study of 46 cases followed through puberty. Journal of Autism and Developmental Disorders 17:273–287. doi: 10.1007/BF01495061.
27. Glykys J, Peng Z, Chandra D, Homanics GE, Houser CR, Mody I. 2007. A new naturally occurring GABA(A) receptor subunit partnership with high sensitivity to ethanol. Nature Neuroscience 10:40–48. doi: 10.1038/nn1813.
28. González-Ramírez MM, Velázquez-Zamora DA, Olvera-Cortés ME, González-Burgos I. 2014. Changes in the plastic properties of hippocampal dendritic spines underlie the attenuation of place learning in healthy aged rats. Neurobiology of Learning and Memory 109:94–103. doi: 10.1016/j.nlm.2013.11.017.
29. Han D, Xu L, Xiao H, Prado Schmidt GC, Shi S. 2013. Dizocilpine reduces head diameter of dendritic spines in the hippocampus of adolescent rats. Psychiatry Research 210:351–356. doi: 10.1016/j.psychres.2013.04.025.
30. Harvey CD, Svoboda K. 2007. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450:1195–1200. doi: 10.1038/nature06416.
31. Heinen K, Baker RE, Spijker S, Rosahl T, van Pelt J, Brussaard AB. 2003. Impaired dendritic spine maturation in GABAA receptor alpha1 subunit knock out mice. Neuroscience 122:699–705. doi: 10.1016/S0306-4522(03)00477-9.
32. Hill TC, Zito K. 2013. LTP-induced long-term stabilization of individual nascent dendritic spines. Journal of Neuroscience 33:2013 33678–686. doi: 10.1523/JNEUROSCI.1404-12.2013.
33. Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K. 2006. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441:979–983. doi: 10.1038/nature04783.
34. Hutsler JJ, Zhang H. 2010. Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Research 1309:83–94. doi: 10.1016/j.brainres.2009.09.120.
35. Huttenlocher PR. 1979. Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Research 163:195–205. doi: 10.1016/0006-8993(79)90349-4.
36. Iacono WG, Beiser M. 1992. Are males more likely than females to develop schizophrenia? The American Journal of Psychiatry 149:1070–1074. doi: 10.1176/ajp.149.8.1070.
37. 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.
38. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H. 2003. Structure-stability-function relationships of dendritic spines. Trends in Neurosciences 26:360–368. doi: 10.1016/S0166-2236(03)00162-0.
39. Kawaguchi Y, Kubota Y. 1997. Gabaergic cell subtypes and their synaptic connections in rat frontal cortex. Cerebral Cortex 7:476–486. doi: 10.1093/cercor/7.6.476.
40. Kitanishi T, Ikegaya Y, Matsuki N, Yamada MK. 2009. Experience-dependent, rapid structural changes in hippocampal pyramidal cell spines. Cerebral Cortex 19:2572–2578. doi: 10.1093/cercor/bhp012.
41. Knutson DC, Mitzey AM, Talton LE, Clagett-Dame M. 2016. Mice null for NEDD9 (HEF1) display extensive hippocampal dendritic spine loss and cognitive impairment. Brain Research 1632:141–155. doi: 10.1016/j.brainres.2015.12.005.
42. Koistinaho M, Ort M, Cimadevilla JM, Vondrous R, Cordell B, Koistinaho J, Bures J, Higgins LS. 2001. Specific spatial learning deficits become severe with age in beta -amyloid precursor protein transgenic mice that harbor diffuse beta -amyloid deposits but do not form plaques. Proceedings of the National Academy of Sciences of the United States of America 98:14675–14680. doi: 10.1073/pnas.261562998.
43. Kopec CD, Li B, Wei W, Boehm J, Malinow R. 2006. Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. Journal of Neuroscience 26:2006:2000–2009. doi: 10.1523/JNEUROSCI.3918-05.2006.
44. Koss WA, Belden CE, Hristov AD, Juraska JM. 2014. Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse 68:61–72. doi: 10.1002/syn.21716.
45. Larson J, Wong D, Lynch G. 1986. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Research 368:347–350. doi: 10.1016/0006-8993(86)90579-2.
46. Ma DQ, Whitehead PL, Menold MM, Martin ER, Ashley-Koch AE, Mei H, Ritchie MD, Delong GR, Abramson RK, Wright HH, Cuccaro ML, Hussman JP, Gilbert JR, Pericak-Vance MA. 2005. Identification of significant association and gene-gene interaction of GABA receptor subunit genes in autism. American Journal of Human Genetics 77:377–388. doi: 10.1086/433195.
47. Ma XM, Huang J, Wang Y, Eipper BA, Mains RE. 2003. Kalirin, a multifunctional rho guanine nucleotide exchange factor, is necessary for maintenance of hippocampal pyramidal neuron dendrites and dendritic spines. Journal of Neuroscience 23:10593–10603.
48. Ma XM, Huang JP, Kim EJ, Zhu Q, Kuchel GA, Mains RE, Eipper BA. 2011. Kalirin-7, an important component of excitatory synapses, is regulated by estradiol in hippocampal neurons. Hippocampus 21:661–677. doi: 10.1002/hipo.20780.
49. Ma XM, Kiraly DD, Gaier ED, Wang Y, Kim EJ, Levine ES, Eipper BA, Mains RE. 2008. Kalirin-7 is required for synaptic structure and function. Journal of Neuroscience 28:12368–12382. doi: 10.1523/JNEUROSCI.4269-08.2008.
50. Ma XM, Miller MB, Vishwanatha KS, Gross MJ, Wang Y, Abbott T, Lam TT, Mains RE, Eipper BA. 2014. Nonenzymatic domains of kalirin7 contribute to spine morphogenesis through interactions with phosphoinositides and abl. Molecular Biology of the Cell 25:1458–1471. doi: 10.1091/mbc.E13-04-0215.
51. Marty MS, Crissman JW, Carney EW. 2001. Evaluation of the male pubertal onset assay to detect testosterone and steroid biosynthesis inhibitors in CD rats. Toxicological Sciences 60:285–295. doi: 10.1093/toxsci/60.2.285.
52. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. 2001. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nature Neuroscience 4:1086–1092. doi: 10.1038/nn736.
53. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429:761–766. doi: 10.1038/nature02617.
54. Nicholls RE, Alarcon JM, Malleret G, Carroll RC, Grody M, Vronskaya S, Kandel ER. 2008. Transgenic mice lacking nmdar-dependent LTD exhibit deficits in behavioral flexibility. Neuron 58:104–117. doi: 10.1016/j.neuron.2008.01.039.
55. Nägerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T. 2004. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44:759–767. doi: 10.1016/j.neuron.2004.11.016.
56. Oaks AW, Zamarbide M, Tambunan DE, Santini E, Di Costanzo S, Pond HL, Johnson MW, Lin J, Gonzalez DM, Boehler JF, Wu GK, Klann E, Walsh CA, Manzini MC. 2016. Cc2d1a loss of function disrupts functional and morphological development in forebrain neurons leading to cognitive and social deficits. Cerebral Cortex. doi: 10.1093/cercor/bhw009.
57. Pastalkova E. 2006. Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141–1144. doi: 10.1126/science.1128657.
58. Penzes P, Johnson RC, Sattler R, Zhang X, Huganir RL, Kambampati V, Mains RE, Eipper BA. 2001. The neuronal rho-gef kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 29:229–242. doi: 10.1016/S0896-6273(01)00193-3.
59. Petanjek Z, Judaš M, Šimic G, Rasin MR, Uylings HB, Rakic P, Kostovic I, Šimic G, Kostovic I. 2011. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proceedings of the National Academy of Sciences of the United States of America 108:13281–13286. doi: 10.1073/pnas.1105108108.
60. Ramerstorfer J, Furtmüller R, Vogel E, Huck S, Sieghart W. 2010. The point mutation gamma 2F77I changes the potency and efficacy of benzodiazepine site ligands in different GABAA receptor subtypes. European Journal of Pharmacology 636:18–27. doi: 10.1016/j.ejphar.2010.03.015.
61. Roussignol G, Ango F, Romorini S, Tu JC, Sala C, Worley PF, Bockaert J, Fagni L. 2005. Shank expression is sufficient to induce functional dendritic spine synapses in aspiny neurons. Journal of Neuroscience 25:3560–3570. doi: 10.1523/JNEUROSCI.4354-04.2005.
62. Sabaliauskas N, Shen H, Homanics GE, Smith SS, Aoki C. 2012. Knockout of the g-aminobutyric acid receptor subunit a4 reduces functional d-containing extrasynaptic receptors in hippocampal pyramidal cells at the onset of puberty. Brain Research 1450:11–23. doi: 10.1016/j.brainres.2012.02.035.
63. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B. 2012. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691–705. doi: 10.1016/j.neuron.2012.03.026.
64. Sekar A, Bialas AR, de Rivera H, Davis A, Hammond TR, Kamitaki N, Tooley K, Presumey J, Baum M, Van Doren V, Genovese G, Rose SA, Handsaker RE, Daly MJ, Carroll MC, Stevens B, McCarroll SA. 2016. Schizophrenia risk from complex variation of complement component 4. Nature 530:177–183. doi: 10.1038/nature16549.
65. Shen H, Gong QH, Aoki C, Yuan M, Ruderman Y, Dattilo M, Williams K, Smith SS. 2007. Reversal of neurosteroid effects at alpha4beta2delta GABA-A receptors triggers anxiety at puberty. Nature Neuroscience 10:469–477. doi: 10.1038/nn1868.
66. Shen H, Sabaliauskas N, Sherpa A, Fenton AA, Stelzer A, Aoki C, Smith SS. 2010. A critical role for alpha4betadelta GABA-A receptors in shaping learning deficits at puberty in mice. Science 327:1515–1518. doi: 10.1126/science.1184245.
67. Shen H, Sabaliauskas N, Yang L, Aoki C, Smith SS. 2016. Role of a4-containing GABA-A receptors in limiting synaptic plasticity and spatial learning of female mice during the pubertal period. Brain Research. doi: 10.1016/j.brainres.2016.01.020.
68. Shi Q, Colodner KJ, Matousek SB, Merry K, Hong S, Kenison JE, Frost JL, Le KX, Li S, Dodart JC, Caldarone BJ, Stevens B, Lemere CA. 2015. Complement c3-deficient mice fail to display age-related hippocampal decline. Journal of Neuroscience 35:13029–13042. doi: 10.1523/JNEUROSCI.1698-15.2015.
69. Sigel E. 2002. Mapping of the benzodiazepine recognition site on GABA(A) receptors. Current Topics in Medicinal Chemistry 2:833–839. doi: 10.2174/1568026023393444.
70. Sigman M, McGovern CW. 2005. Improvement in cognitive and language skills from preschool to adolescence in autism. Journal of Autism and Developmental Disorders 35:15–23. doi: 10.1007/s10803-004-1027-5.
71. Spiga S, Talani G, Mulas G, Licheri V, Fois GR, Muggironi G, Masala N, Cannizzaro C, Biggio G, Sanna E, Diana M. 2014. Hampered long-term depression and thin spine loss in the nucleus accumbens of ethanol-dependent rats. Proceedings of the National Academy of Sciences of the United States of America 111:E3745–3754. doi: 10.1073/pnas.1406768111.
72. Stell BM, Mody I. 2002. Receptors with different affinities mediate phasic and tonic GABA(A) conductances in hippocampal neurons. Journal of Neuroscience 22.
73. Tang G, Gudsnuk K, Kuo SH, Cotrina ML, Rosoklija G, Sosunov A, Sonders MS, Kanter E, Castagna C, Yamamoto A, Yue Z, Arancio O, Peterson BS, Champagne F, Dwork AJ, Goldman J, Sulzer D. 2014. Loss of mtor- dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron 83:1131–1143. doi: 10.1016/j.neuron.2014.07.040.
74. Thomases DR, Cass DK, Tseng KY. 2013. Periadolescent exposure to the NMDA receptor antagonist MK-801 impairs the functional maturation of local gabaergic circuits in the adult prefrontal cortex. Journal of Neuroscience 33:2013:26–34. doi: 10.1523/JNEUROSCI.4147-12.2013.
75. Turner AM, Greenough WT. 1985. Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Research 329:195–203. doi: 10.1016/0006-8993(85)90525-6
76. van Spronsen M, Hoogenraad CC. 2010. Synapse pathology in psychiatric and neurologic disease. Current Neurology and Neuroscience Reports 10:207–214. doi: 10.1007/s11910-010-0104-8.
77. Verleye M, Heulard I, Gillardin JM. 2008. Investigation of the anticonvulsive effect of acute immobilization stress in anxious balb/cbyj mice using GABA a-related mechanistic probes. Psychopharmacology 197:523–534. doi: 10.1007/s00213-007-1066-7.
78. Wang HX, Gao WJ. 2012. Prolonged exposure to NMDAR antagonist induces cell-type specific changes of glutamatergic receptors in rat prefrontal cortex. Neuropharmacology 62:1808–1822. doi: 10.1016/j.neuropharm.2011.11.024.
79. Wiesmann UN, DiDonato S, Herschkowitz NN. 1975. Effect of chloroquine on cultured fibroblasts: Release of lysosomal hydrolases and inhibition of their uptake. Biochemical and Biophysical Research Communications 66. doi: 10.1016/0006-291X(75)90506-9.
80. Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA. 1997. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: Correlation with dendritic spine density. Journal of Neuroscience 17:1848–1859.
81. Xi D, Zhang W, Wang HX, Stradtman GG, Gao WJ. 2009. Dizocilpine (MK-801) induces distinct changes of n- methyl-d-aspartic acid receptor subunits in parvalbumin-containing interneurons in young adult rat prefrontal cortex. The International Journal of Neuropsychopharmacology 12:1395–1408. doi: 10.1017/S146114570900042X
82. Yildirim M, Mapp OM, Janssen WG, Yin W, Morrison JH, Gore AC. 2008. Postpubertal decrease in hippocampal dendritic spines of female rats. Experimental Neurology 210:339–348. doi: 10.1016/j.expneurol.2007.11.003.
83. Zehr JL, Todd BJ, Schulz KM, McCarthy MM, Sisk CL. 2006. Dendritic pruning of the medial amygdala during pubertal development of the male syrian hamster. Journal of Neurobiology 66:578–590. doi: 10.1002/neu.20251.
84. Zolkowska D, Banks CN, Dhir A, Inceoglu B, Sanborn JR, McCoy MR, Bruun DA, Hammock BD, Lein PJ, Rogawski MA. 2012. Characterization of seizures induced by acute and repeated exposure to tetramethylenedisulfotetramine. The Journal of Pharmacology and Experimental Therapeutics 341:435–446. doi: 10.1124/jpet.111.190579.
85. Zurek AA, Bridgwater EM, Orser BA. 2012. Inhibition of a5 g-aminobutyric acid type A receptors restores recognition memory after general anesthesia. Anesthesia and Analgesia 114:845–855. doi: 10.1213/ANE.0b013e31824720da