Activation of the G protein-coupled estrogen receptor, but not estrogen receptor α or β, rapidly enhances social learning

Psychoneuroendocrinology

Volumn 58, Issue , 2015, Pages 51-66

  Ervin, Kelsy Sharice Jean ^a   Mulvale, Erin ^a   Gallagher, Nicola ^a   Roussel, Véronique ^a   Choleris, Elena ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Estradiol; Estrogen receptor alpha; Estrogen receptor beta; GPER; GPR30; Rapid estrogen effects; Social transmission of food preferences

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED ESTROGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 30; UNCLASSIFIED DRUG; 1,3,5-TRIS(4-HYDROXYPHENYL)-4-PROPYL-1H-PYRAZOLE; GPR30 PROTEIN, MOUSE; NITRILE; PHENOL DERIVATIVE; PROPIONIC ACID DERIVATIVE; PYRAZOLE DERIVATIVE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CACAO; CINNAMON; CONTROLLED STUDY; DOSE RESPONSE; ESTRUS CYCLE; FACILITATION; FEMALE; FOOD INTAKE; FOOD PREFERENCE; MOUSE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RECEPTOR BINDING; SOCIAL INTERACTION; SOCIAL LEARNING; SOCIAL TRANSMISSION OF FOOD PREFERENCES; TASK PERFORMANCE; AGONISTS; ANIMAL; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

ANIMALS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; MICE; NITRILES; PHENOLS; PROPIONATES; PYRAZOLES; RECEPTORS, G-PROTEIN-COUPLED; SOCIAL LEARNING;

EID: 84933061022     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.04.002     Document Type: Article

References (107)

1. Alvarez P., Lipton P.A., Melrose R., Eichenbaum H. Differential effects of damage within the hippocampal region on memory for a natural, nonspatial odor-odor association. Learn. Mem. 2001, 8:79-86.
2. Bandura A. Human agency in social cognitive theory. Am. Psychol. 1989, 44:1175-1184.
3. Berger-Sweeney J., Stearns N.A., Frick K.M., Beard B., Baxter M.G. Cholinergic basal forebrain is critical for social transmission of food preferences. Hippocampus 2000, 10:729-738.
4. Boix-Trelis N., Vale-Martínez A., Guillazo-Blanch G., Martí-Nicolovius M. Muscarinic cholinergic receptor blockade in the rat prelimbic cortex impairs the social transmission of food preference. Neurobiol. Learn. Mem. 2007, 87:659-668.
5. Boix-Trelis N., Vale-Martinez A., Guillazo-Blanch G., Costa-Miserachs D., Marti-Nicolovius M. Effects of nucleus basalis magnocellularis stimulation on a socially transmitted food preference and c-Fos expression. Learn. Mem. 2006, 13:783-793.
6. Bologa C.G., Revankar C.M., Young S.M., Edwards B.S., Arterburn J.B., Kiselyov A.S., Parker M.A., Tkachenko S.E., Savchuck N.P., Sklar L.A., Oprea T.I., Prossnitz E.R. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol. 2006, 2:207-212.
7. Boulware M.I., Heisler J.D., Frick K.M. The memory-enhancing effects of hippocampal estrogen receptor activation involve metabotropic glutamate receptor signaling. J. Neurosci. 2013, 33:15184-15194.
8. Brailoiu E., Dun S.L., Brailoiu G.C., Mizuo K., Sklar L.A., Oprea T.I., Prossnitz E.R., Dun N.J. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 2007, 193:311-321.
9. Brown C., Laland K.N. Social learning in fishes: a review. Fish Fish. 2003, 4:280-288.
10. Bunsey M., Eichenbaum H. Selective damage to the hippocampal region blocks long-term retention of a natural and nonspatial stimulus-stimulus association. Hippocampus 1995, 5:546-556.
11. Burton S., Murphy D., Qureshi U., Sutton P., O'Keefe J. Combined lesions of hippocampus and subiculum do not produced deficits in a nonspatial social olfactory memory task. J. Neurosci. 2000, 20:5468-5475.
12. Byers S.L., Wiles M.V., Dunn S.L., Taft R.A. Mouse estrous cycle identification tool and images (mouse estrous cycle identification). PLoS ONE 2012, 7:e35538.
13. Cain D., Finlayson C., Boon F., Beiko J. Ethanol impairs behavioral strategy use in naive rats but does not prevent spatial learning in the water maze in pretrained rats. Psychopharmacology 2002, 164:1-9.
14. Carballo-Marquez A., Vale-Martinez A., Guillazo-Blanch G., Marti-Nicolovius M. Muscarinic transmission in the basolateral amygdala is necessary for the acquisition of socially transmitted food preferences in rats. Neurobiol. Learn. Mem. 2009, 91:98-101.
15. Carmeci C., Thompson D.A., Ring H.Z., Francke U., Weigel R.J. Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer. Genomics 1997, 45:607-617.
16. Cashdan E. Adaptiveness of food learning and food aversions in children. Soc. Sci. Inf. 1998, 37:613-632.
17. Choleris E., Clipperton Allen A.E., Phan A., Kavaliers M. Neuroendocrinology of social information processing in rats and mice. Front. Neuroendocrinol. 2009, 30:442-459.
18. Choleris E., Clipperton-Allen A., Phan A., Valsecchi P., Kavaliers M. Estrogenic involvement in social learning, social recognition and pathogen avoidance. Front. Neuroendocrinol. 2012, 33:140-159.
19. Choleris E., Clipperton A.E., Gray D.G., Diaz-Gonzalez S., Welsman R.G. Differential effects of dopamine receptor D1-type and D2-type antagonists and phase of the estrous cycle on social learning of food preferences, feeding, and social interactions in mice. Neuropsychopharmacology 2011, 36:1689-1702.
20. Choleris E., Cazzin L., Lymer J.M., Amor T.R., Lu R., Kavaliers M., Valsecchi P. Acute corticosterone sexually dimorphically facilitates social learning and inhibits feeding in mice. Neuropharmacology 2013, 75:191-200.
21. Clipperton Allen A.E., Cragg C.L., Wood A.J., Pfaff D.W., Choleris E. Agonistic behavior in males and females: effects of an estrogen receptor beta agonist in gonadectomized and gonadally intact mice. Psychoneuroendocrinology 2010, 35:1008-1022.
22. Clipperton A.E., Spinato J.M., Chernets C., Pfaff D.W., Choleris E. Differential effects of estrogen receptor alpha and beta specific agonists on social learning of food preferences in female mice. Neuropsychopharmacology 2008, 33:2362-2375.
23. Clipperton-Allen A., Almey A., Melichercik A., Allen C.P., Choleris E. Effects of an estrogen receptor alpha agonist on agonistic behaviour in intact and gonadectomized male and female mice. Psychoneuroendocrinology 2011, 36:981-995.
24. Crawley J.N., Crawley J.N. Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol. 2007, 17:448-459.
25. Ervin K.S.J., Phan A., Gabor C.S., Choleris E. Rapid oestrogenic regulation of social and nonsocial learning. J. Neuroendocrinol. 2013, 25:1116-1132.
26. Fernandez S.M., Lewis M.C., Pechenino A.S., Harburger L.L., Orr P.T., Gresack J.E., Schafe G.E., Frick K.M. Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J. Neurosci. 2008, 28:8660.
27. Filardo E.J., Quinn J.A., Bland K.I., Frackleton A.R. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 2000, 14:1649-1660.
28. Fortress A.M., Fan L., Orr P.T., Zhao Z., Frick K.M. Estradiol-induced object recognition memory consolidation is dependent on activation of mTOR signaling in the dorsal hippocampus. Learn. Mem. 2013, 20:147-155.
29. Frye C.A., Duffy C.K., Walf A.A. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol. Learn. Mem. 2007, 88:208-216.
30. Galef B., Stein M. Demonstrator influence on observer diet preference: analyses of critical social interactions and olfactory signals. Anim. Learn. Behav. 1985, 13:31-38.
31. Galef B.G. An adaptationist perspective on social learning, social feeding and social foraging in Norway rats. Contemporary Issues in Comparative Psychology 1989, 55-79. Sinauer Associates, Sunderland, MA. D.A. Dewsbury (Ed.).
32. Galef B.G. Social enhancement of food preferences in Norway rats: a brief review. Social Learning in Animals: The Roots of Culture 1996, 49-64. Academic Press, San Diego, CA. C. Heyes, B.G. Galef (Eds.).
33. Galef B.G.J., Wigmore S.W. Transfer of information concerning distant foods: a laboratory investigation of the "information-centre" hypothesis. Anim. Behav. 1983, 31:748-758.
34. Galef B.G.J., Kennett D.J., Wigmore S.W. Transfer of information concerning distant food in rats: a robust phenomenon. Anim. Learn. Behav. 1984, 12:292-296.
35. Galef B.G.J., Kennett D.J., Stein M. Demonstrator influence on observer diet preference: effects of simple exposure and the presence of a demonstrator. Anim. Learn. Behav. 1985, 13:25-30.
36. Gallate J., Morley K., Ambermoon P., McGregor I. The consequences of beer consumption in rats: acute anxiolytic and ataxic effects and withdrawal-induced anxiety. Psychopharmacology 2003, 166:51-60.
37. Geary N., Asarian L., Korach K.S., Pfaff D.W., Ogawa S. Deficits in E2-dependent control of feeding, weight gain, and cholecystokinin satiation in ER-α null mice. Endocrinology 2001, 142:4751-4757.
38. Gibbs R.B., Nelson D., Hammond R. Role of GPR30 in mediating estradiol effects on acetylcholine release in the hippocampus. Horm. Behav. 2014, 66:339-345.
39. Gold P.E., Countryman R.A., Dukala D., Chang Q. Acetylcholine release in the hippocampus and prelimbic cortex during acquisition of a socially transmitted food preference. Neurobiol. Learn. Mem. 2011, 96:498-503.
40. Gould T.J., Leach P.T. Cellular, molecular, and genetic substrates underlying the impact of nicotine on learning. Neurobiol. Learn. Mem. 2014, 107:108-132.
41. Grant E.C., Mackintosh J.H. A comparison of the social postures of some common laboratory rodents. Behaviour 1963, 21:246-259.
42. Gresack J.E., Frick K.M. Effects of continuous and intermittent estrogen treatments on memory in aging female mice. Brain Res. 2006, 1115:135-147.
43. Griffin A.S. Social learning about predators: a review and prospectus. Learn. Behav. 2004, 32:131-140.
44. Hammond R., Gibbs R.B. GPR30 is positioned to mediate estrogen effects on basal forebrain cholinergic neurons and cognitive performance. Brain Res. 2011, 1379:53-60.
45. Hammond R., Nelson D., Gibbs R.B. GPR30 co-localizes with cholinergic neurons in the basal forebrain and enhances potassium-stimulated acetylcholine release in the hippocampus. Psychoneuroendocrinology 2011, 36:182-192.
46. Hammond R., Nelson D., Kline E., Gibbs R.B. Chronic treatment with a GPR30 antagonist impairs acquisition of a spatial learning task in young female rats. Horm. Behav. 2012, 62:367-374.
47. Hammond R., Mauk R., Ninaci D., Nelson D., Gibbs R.B. Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm. Behav. 2009, 56:309-314.
48. Harburger L.L., Saadi A., Frick K.M. Dose-dependent effects of post-training estradiol plus progesterone treatment on object memory consolidation and hippocampal extracellular signal-regulated kinase activation in young ovariectomized mice. Neuroscience 2009, 160:6-12.
49. Hartung C.M., Widiger T.A. Gender differences in the diagnosis of mental disorders: conclusions and controversies of the DSM-IV. Psychol. Bull. 1998, 123:260-278.
50. Hawley W.R., Grissom E.M., Moody N.M., Dohanich G.P., Vasudevan N. Activation of G-protein-coupled receptor 30 is sufficient to enhance spatial recognition memory in ovariectomized rats. Behav. Brain Res. 2014, 262:68-73.
51. Heine P., Taylor J., Iwamoto G., Lubahn D., Cooke P. Increased adipose tissue in male and female estrogen receptor-α knockout mice. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:12729-12734.
52. Heldring N., Pike A., Andersson S., Cheng G., Matthews J., Hartman J., Tujague M., Strom A., Treuter E., Warner M., Gustafsson J. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 2007, 87:905-931.
53. Iizuka S., Ishige A., Komatsu Y., Matsumiya T., Inazu M., Takeda H. Effects of Toki-shakuyaku-san on electric footshock stress in ovariectomized mice. Methods Find. Exp. Clin. Pharmacol. 1998, 20:39-46.
54. Inagaki T., Gautreaux C., Luine V. Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm. Behav. 2010, 58:415-426.
55. Jacome L.F., Gautreaux C., Inagaki T., Mohan G., Alves S., Lubbers L.S., Luine V. Estradiol and ERβ agonists enhance recognition memory, and DPN, an ERβ agonist, alters brain monoamines. Neurobiol. Learn. Mem. 2010, 94:488-498.
56. Kelly M.J., Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 2001, 12:152-156.
57. Kelly M.J., Rønnekleiv O.K. Membrane-initiated estrogen signaling in hypothalamic neurons. Mol. Cell. Endocrinol. 2008, 290:14-23.
58. Lesburguères E., Gobbo O.L., Alaux-Cantin S., Hambucken A., Trifilieff P., Bontempi B. Early tagging of cortical networks is required for the formation of enduring associative memory. Science 2011, 331:924-925.
59. Luine V.N., Jacome L.F., Maclusky N.J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 2003, 144:2836-2844.
60. Luine V.N., Frankfurt M. Estrogens facilitate memory processing through membrane mediated mechanisms and alterations in spine density. Front. Neuroendocrinol. 2012, 33:388-402.
61. Luine V.N. Estradiol and cognitive function: past, present and future. Horm. Behav. 2014, 66:602-618.
62. Mendoza-Garcés L., Mendoza-Rodríguez C.A., Jiménez-Trejo F., Picazo O., Rodríguez M.C., Cerbón M. Differential expression of estrogen receptors in two hippocampal regions during the estrous cycle of the rat. Anat. Rec. 2011, 294:1913-1919.
63. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., Katzenellenbogen J.A. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J. Med. Chem. 2001, 44:4230-4251.
64. Micevych P., Dominguez R. Membrane estradiol signaling in the brain. Front. Neuroendocrinol. 2009, 30:315-327.
65. Micevych P., Kelly M.J. Membrane estrogen receptor regulation of hypothalamic function. Neuroendocrinology 2012, 96:103-110.
66. Moss R.L., Gu Q. Estrogen: mechanisms for a rapid action in CA1 hippocampal neurons. Steroids 1999, 64:14-21.
67. Musatov S., Chen W., Pfaff D.W., Mobbs C.V., Yang X.J., Clegg D.J., Kaplitt M.G., Ogawa S. Silencing of estrogen receptor alpha in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2501-2506.
68. Nagell K., Olguin R.S., Tomasello M. Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens). J. Comp. Psychol. 1993, 107:174-186.
69. Nilsson S., Koehler K.F., Gustafsson J.-A. Development of subtype-selective oestrogen receptor-based therapeutics. Nat. Rev. Drug Discov. 2011, 10:778-792.
70. Noel S.D., Keen K.L., Baumann D.I., Filardo E.J., Terasawa E. Involvement of G protein-coupled receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons. Mol. Endocrinol. 2009, 23:349-359.
71. Phan A., Gabor C.S., Favaro K.J., Kaschack S., Armstrong J.N., Maclusky N.J., Choleris E. Low doses of 17β-Estradiol rapidly improve learning and increase hippocampal dendritic spines. Neuropsychopharmacology 2012, 37:2299-2309.
72. Phan A., Phan L., Lancaster A., Armstrong K.E., MacLusky J.N., Choleris N.J.E. Rapid effects of estrogen receptor alpha and beta selective agonists on learning and dendritic spines in female mice. Endocrinology 2011, 152:1492-1502.
73. Ponomarev I., Crabbe J.C. A novel method to assess initial sensitivity and acute functional tolerance to hypnotic effects of ethanol. J. Pharmacol. Exp. Ther. 2002, 302:257-263.
74. Rhodes M.E., Frye C.A. Estrogen has mnemonic-enhancing effects in the inhibitory avoidance task. Pharmacol. Biochem. Behav. 2004, 78:551-558.
75. Rhodes M.E., Frye C.A. ER beta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiol. Learn. Mem. 2006, 85:183-191.
76. Roepke T.A., Rønnekleiv O.K., Kelly M.J. Physiological consequences of membrane-initiated estrogen signalling in the brain. Front. Biosci. 2011, 16:1560-1573.
77. Roesch D.M. Effects of selective estrogen receptor agonists on food intake and body weight gain in rats. Physiol. Behav. 2006, 87:39-44.
78. Rosenberg T., Gal-Ben-Ari S., Dietrich D.C., Kreutz M.R., Ziv N.E., Gundelfinger E.D., Rosenblum K. The roles of protein expression in synaptic plasticity and memory consolidation. Front. Mol. Neurosci. 2014, 7. 10.3389/fnmol.2014.00086.
79. Ross R.S., Eichenbaum H. Dynamics of hippocampal and cortical activation during consolidation of a nonspatial memory. J. Neurosci. 2006, 26:4852-4859.
80. Ross R.S., McGaughy J., Eichenbaum H. Acetylcholine in the orbitofrontal cortex is necessary for the acquisition of a socially transmitted food preference. Learn. Mem. 2005, 12:302-306.
81. Rudy J.W. Actin dynamics and the evolution of the memory trace. Brain Res. 2014, 10.1016/j.brainres.2014.12.007.
82. Ryabinin A.E., Miller M.N., Durrant S. Effects of acute alcohol administration on object recognition learning in C57BL/6J mice. Pharmacol. Biochem. Behav. 2002, 71:307-312.
83. Sánchez-Andrade G., James B.M., Kendrick K.M. Neural encoding of olfactory recognition memory. J. Reprod. Dev. 2005, 51:547-558.
84. Santollo J., Wiley M.D., Eckel L.A. Acute activation of ERα decreases food intake, meal size, and body weight in ovariectomized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R2194-R2201.
85. Santollo J., Marshall A., Daniels D. Activation of membrane-associated estrogen receptors decreases food and water intake in ovariectomized rats. Endocrinology 2013, 154:320-329.
86. Santollo J., Yao D., Neal-Perry G., Etgen A.M. Middle-aged female rats retain sensitivity to the anorexigenic effect of exogenous estradiol. Behav. Brain Res. 2012, 232:159-164.
87. Sarkar S.N., Sarkar S., Smith S.N., Logan L.T., Simpkins S.M.J.W. Estrogen-induced activation of extracellular signal-regulated kinase signaling triggers dendritic resident mRNA translation. Neuroscience 2010, 170:1080-1085.
88. Scharfman H.E., Hintz T.M., Gomez J., Stormes K.A., Barouk S., Malthankar-phatak G.H., Mccloskey D.P., Luine V.N., Maclusky N.J. Changes in hippocampal function of ovariectomized rats after sequential low doses of estradiol to simulate the preovulatory estrogen surge. Eur. J. Neurosci. 2007, 26:2595-2612.
89. Smith C.A., Countryman R.A., Sahuque L.L., Colombo P.J. Time-courses of Fos expression in rat hippocampus and neocortex following acquisition and recall of a socially transmitted food preference. Neurobiol. Learn. Mem. 2007, 88:65-74.
90. Spiteri T., Musatov S., Ogawa S., Ribeiro A., Pfaff D.W., Ågmo A. The role of the estrogen receptor α in the medial amygdala and ventromedial nucleus of the hypothalamus in social recognition, anxiety and aggression. Behav. Brain Res. 2010, 210:211-220.
91. Srivastava D.P. Two-Step Wiring Plasticity - a mechanism for estrogen-induced rewiring of cortical circuits. J. Steroid Biochem. Mol. Biol. 2012, 131:17-23.
92. Stauffer S.R., Huang Y.R., Aron Z.D., Coletta C.J., Sun J., Katzenellenbogen B.S., Katzenellenbogen J.A. Triarylpyrazoles with basic side chains: development of pyrazole-based estrogen receptor antagonists. Bioorg. Med. Chem. 2001, 9:151-161.
93. Sugiyama N., Barros R.P., Warner M., Gustafsson J.-A. ERbeta: recent understanding of estrogen signaling. Trends Endocrinol. Metab. 2010, 21:545-552.
94. Terasawa E., Noel S.D., Keen K.L. Rapid action of estrogen in LHRH neurons: the role of GPR30. J. Neuroendocrinol. 2009, 21:316-321.
95. Thapa R., Sparks F.T., Hanif W., Gulbrandsen T., Sutherland R.J. Recent memory for socially transmitted food preferences in rats does not depend on the hippocampus. Neurobiol. Learn. Mem. 2014, 114:113-116.
96. Thomas P., Pang Y., Filardo E.J., Dong J. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 2005, 146:624-632.
97. Tuscher J.J., Fortress A.M., Kim J., Frick K.M. Regulation of object recognition and object placement by ovarian sex steroid hormones. Behav. Brain Res. 2014, 10.1016/j.bbr.2014.08.001.
98. Valsecchi P., Galef B.G.J. Social influences on the food preferences of house mice (Mus musculus). Int. J. Comp. Psychol. 1989, 2:245-256.
99. Vasudevan N., Pfaff D.W. Membrane-initiated actions of estrogens in neuroendocrinology: emerging principles. Endocr. Rev. 2007, 28:1-19.
100. Vasudevan N., Pfaff D.W. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front. Neuroendocrinol. 2008, 29:238-257.
101. Waters E.M., Thompson L.I., Patel P., Gonzales A.D., Ye H.Z., Filardo E.J., Clegg D.J., Gorecka J., Akama K.T., McEwen B.S., Milner T.A. G-protein-coupled estrogen receptor 1 is anatomically positioned to modulate synaptic plasticity in the mouse hippocampus. J. Neurosci. 2015, 35:2384-2397.
102. Whiten A., Flynn E. The transmission and evolution of experimental microcultures in groups of young children. Dev. Psychol. 2010, 46:1694-1709.
103. Winocur G. Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions. Behav. Brain Res. 1990, 38:145-154.
104. Winters B.D., Saksida L.M., Bussey T.J. Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci. Biobehav. Rev. 2008, 32:1055-1070.
105. Wong M., Moss R.L. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J. Neurosci. 1992, 12:3217-3225.
106. Wong M., Thompson T.L., Moss R.L. Nongenomic actions of estrogen in the brain: physiological significance and cellular mechanisms. Crit. Rev. Neurobiol. 1996, 10:189-203.
107. Yeung H.H., Werker J.F. Learning words' sounds before learning how words sound: 9-month-olds use distinct objects as cues to categorize speech information. Cognition 2009, 113:234-243.