Docosahexaenoic acid partially ameliorates deficits in social behavior and ultrasonic vocalizations caused by prenatal ethanol exposure

Behavioural Brain Research

Volumn 286, Issue , 2015, Pages 201-211

  Wellmann, Kristen A ^a   George, Finney ^a   Brnouti, Fares ^a   Mooney, Sandra M ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

DHA; Fetal alcohol syndrome; Omega 3 polyunsaturated fatty acid; Social interaction

Indexed keywords

ALCOHOL; DOCOSAHEXAENOIC ACID; CENTRAL DEPRESSANT AGENT; PSYCHOTROPIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; ARTIFICIAL MILK; CONTROLLED STUDY; DIET SUPPLEMENTATION; ELEVATED PLUS MAZE TEST; EXPERIMENTAL SOCIAL BEHAVIOR TEST; FEMALE; FETAL ALCOHOL SYNDROME; ISOLATION INDUCED ULTRASONIC VOCALIZATION TEST; MALE; MOTOR PERFORMANCE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; SOCIAL INTERACTION; SOMATOSENSORY CORTEX; ANIMAL; DRUG EFFECTS; FETAL ALCOHOL SPECTRUM DISORDERS; LONG EVANS RAT; PREGNANCY; PSYCHOLOGY; RANDOMIZATION; SOCIAL BEHAVIOR; SOCIAL ISOLATION; ULTRASOUND; VOCALIZATION;

ANIMALS; ANXIETY; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DOCOSAHEXAENOIC ACIDS; ETHANOL; FEMALE; FETAL ALCOHOL SPECTRUM DISORDERS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PSYCHOTROPIC DRUGS; RANDOM ALLOCATION; RATS, LONG-EVANS; SOCIAL BEHAVIOR; SOCIAL ISOLATION; ULTRASONICS; VOCALIZATION, ANIMAL;

EID: 84924987802     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.02.048     Document Type: Article

References (106)

1. Thomas S.E., Kelly S.J., Mattson S.N., Riley E.P. Comparison of social abilities of children with fetal alcohol syndrome to those of children with similar IQ scores and normal controls. Alcohol Clin Exp Res 1998, 22:528-533.
2. Kelly S.J., Day N., Streissguth A.P. Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicol Teratol 2000, 22:143-149.
3. Roebuck T.M., Mattson S.N., Riley E.P. Behavioral and psychosocial profiles of alcohol-exposed children. Alcohol Clin Exp Res 1999, 23:1070-1076.
4. Whaley S.E., O'Connor And M.J., Gunderson B. Comparison of the adaptive functioning of children prenatally exposed to alcohol to a nonexposed clinical sample. Alcohol Clin Exp Res 2001, 25:1018-1024.
5. Olson H.C., Feldman J.J., Streissguth A.P., Sampson P.D., Bookstein F.L. Neuropsychological deficits in adolescents with fetal alcohol syndrome: clinical findings. Alcohol Clin Exp Res 1998, 22:1998-2012.
6. Meyer L.S., Riley E.P. Social play in juvenile rats prenatally exposed to alcohol. Teratology 1986, 34:1-7. 10.1002/tera.1420340102.
7. Lugo J.N., Marino M.D., Cronise K., Kelly S.J. Effects of alcohol exposure during development on social behavior in rats. Physiol Behav 2003, 78:185-194.
8. Charles Lawrence R., Cale Bonner H., Newsom R.J., Kelly S.J. Effects of alcohol exposure during development on play behavior and c-Fos expression in response to play behavior. Behav Brain Res 2008, 188:209-218. 10.1016/j.bbr.2007.10.028.
9. Hamilton D.A., Akers K.G., Rice J.P., Johnson T.E., Candelaria-Cook F.T., Maes L.I., et al. Prenatal exposure to moderate levels of ethanol alters social behavior in adult rats: relationship to structural plasticity and immediate early gene expression in frontal cortex. Behav Brain Res 2010, 207:290-304. 10.1016/j.bbr.2009.10.012.
10. Panksepp J., Normansell L., Cox J.F., Siviy S.M. Effects of neonatal decortication on the social play of juvenile rats. Physiol Behav 1994, 56:429-443.
11. Siviy S.M., Panksepp J. Sensory modulation of juvenile play in rats. Dev Psychobiol 1987, 20:39-55. 10.1002/dev.420200108.
12. Miller M.W., Potempa G. Numbers of neurons and glia in mature rat somatosensory cortex: effects of prenatal exposure to ethanol. J Comp Neurol 1990, 293:92-102. 10.1002/cne.902930108.
13. Miller M.W., Dow-Edwards D.L. Vibrissal stimulation affects glucose utilization in the trigeminal/somatosensory system of normal rats and rats prenatally exposed to ethanol. J Comp Neurol 1993, 335:283-284. 10.1002/cne.903350211.
14. Miller M.W., Dow-Edwards D.L. Structural and metabolic alterations in rat cerebral cortex induced by prenatal exposure to ethanol. Brain Res 1988, 474:316-326.
15. Mooney S.M., Miller M.W. Effects of prenatal exposure to ethanol on systems matching: the number of neurons in the ventrobasal thalamic nucleus of the mature rat. Brain Res Dev Brain Res 1999, 117:121-125.
16. Mooney S.M., Miller M.W. Prenatal exposure to ethanol affects postnatal neurogenesis in thalamus. Exp Neurol 2010, 223:566-573. 10.1016/j.expneurol.2010.02.003.
17. Minciacchi D., Granato A., Santarelli M., Sbriccoli A. Modifications of thalamo-cortical circuitry in rats prenatally exposed to ethanol. Neuroreport 1993, 4:415-418.
18. Granato A., Santarelli M., Sbriccoli A., Minciacchi D. Multifaceted alterations of the thalamo-cortico-thalamic loop in adult rats prenatally exposed to ethanol. Anat Embryol (Berl) 1995, 191:11-23.
19. Santarelli M., Granato A., Sbriccoli A., Gobbi G., Janiri L., Minciacchi D. Alterations of the thalamo-cortical system in rats prenatally exposed to ethanol are prevented by concurrent administration of acetyl-l-carnitine. Brain Res 1995, 698:241-247.
20. Vingan R.D., Dow-Edwards D.L., Riley E.P. Cerebral metabolic alterations in rats following prenatal alcohol exposure: a deoxyglucose study. Alcohol Clin Exp Res 1986, 10:22-26.
21. Wainwright P.E. Do essential fatty acids play a role in brain and behavioral development?. Neurosci Biobehav Rev 1992, 16:193-205.
22. Cao D., Kevala K., Kim J., Moon H.S., Jun S.B., Lovinger D., et al. Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J Neurochem 2009, 111:510-521. 10.1111/j.1471-4159.2009.06335.x.
23. Bazan N.G., Musto A.E., Knott E.J. Endogenous signaling by omega-3 docosahexaenoic acid-derived mediators sustains homeostatic synaptic and circuitry integrity. Mol Neurobiol 2011, 44:216-222. 10.1007/s12035-011-8200-6.
24. Furuya H., Watanabe T., Sugioka Y., Inagaki Y., Okazaki I. Effect of ethanol and docosahexaenoic acid on nerve growth factor-induced neurite formation and neuron specific growth-associated protein gene expression in PC12 cells. Nihon Arukoru Yakubutsu Igakkai Zasshi 2002, 37:513-522.
25. Calderon F., Kim H.Y. Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J Neurochem 2004, 90:979-988. 10.1111/j.1471-4159.2004.02520.x.
26. Cao D., Xue R., Xu J., Liu Z. Effects of docosahexaenoic acid on the survival and neurite outgrowth of rat cortical neurons in primary cultures. J Nutr Biochem 2005, 16:538-546. 10.1016/j.jnutbio.2005.02.002.
27. McNamara R.K. Deciphering the role of docosahexaenoic acid in brain maturation and pathology with magnetic resonance imaging. Prostaglandins Leukot Essent Fatty Acids 2013, 88:33-42. 10.1016/j.plefa.2012.03.011.
28. Moriguchi T., Greiner R.S., Salem N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J Neurochem 2000, 75:2563-2573.
29. Fedorova I., Hussein N., Di Martino C., Moriguchi T., Hoshiba J., Majchrzak S., et al. An n-3 fatty acid deficient diet affects mouse spatial learning in the Barnes circular maze. Prostaglandins Leukot Essent Fatty Acids 2007, 77:269-277. 10.1016/j.plefa.2007.10.013.
30. Fedorova I., Hussein N., Baumann M.H., Di Martino C., Salem N. An n-3 fatty acid deficiency impairs rat spatial learning in the Barnes maze. Behav Neurosci 2009, 123:196-205. 10.1037/a0013801.
31. Fedorova I., Alvheim A.R., Hussein N., Salem N. Deficit in prepulse inhibition in mice caused by dietary n-3 fatty acid deficiency. Behav Neurosci 2009, 123:1218-1225. 10.1037/a0017446.
32. Moreira J.D., Knorr L., Ganzella M., Thomazi A.P., de Souza C.G., de Souza D.G., et al. Omega-3 fatty acids deprivation affects ontogeny of glutamatergic synapses in rats: relevance for behavior alterations. Neurochem Int 2010, 56:753-759. 10.1016/j.neuint.2010.02.010.
33. Martinez M., Mougan I. Fatty acid composition of human brain phospholipids during normal development. J Neurochem 1998, 71:2528-2533.
34. Carver J.D., Benford V.J., Han B., Cantor A.B. The relationship between age and the fatty acid composition of cerebral cortex and erythrocytes in human subjects. Brain Res Bull 2001, 56:79-85. 10.1016/S0361-9230(01)00551-2.
35. Brenna J.T., Varamini B., Jensen R.G., Diersen-Schade D.A., Boettcher J.A., Arterburn L.M. Docosahexaenoic and arachidonic acid concentrations in human breast milk worldwide. Am J Clin Nutr 2007, 85:1457-1464.
36. Willatts P., Forsyth J.S., DiModugno M.K., Varma S., Colvin M. Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age. Lancet 1998, 352:688-691.
37. Helland I.B., Smith L., Saarem K., Saugstad O.D., Drevon C.A. Maternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children's IQ at 4 years of age. Pediatrics 2003, 111:e39-e44.
38. Judge M.P., Harel O., Lammi-Keefe C.J. Maternal consumption of a docosahexaenoic acid-containing functional food during pregnancy: benefit for infant performance on problem-solving but not on recognition memory tasks at age 9mo. Am J Clin Nutr 2007, 85:1572-1577.
39. Birch E.E., Garfield S., Hoffman D.R., Uauy R., Birch D.G. A randomized controlled trial of early dietary supply of long-chain polyunsaturated fatty acids and mental development in term infants. Dev Med Child Neurol 2000, 42:174-181.
40. Cohen-Kerem R., Koren G. Antioxidants and fetal protection against ethanol teratogenicity. I. Review of the experimental data and implications to humans. Neurotoxicol Teratol 2003, 25:1-9.
41. Heaton M.B., Mitchell J.J., Paiva M. Amelioration of ethanol-induced neurotoxicity in the neonatal rat central nervous system by antioxidant therapy. Alcohol Clin Exp Res 2000, 24:512-518.
42. Thomas J.D., Garrison M., O'Neill T.M. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 2004, 26:35-45. 10.1016/j.ntt.2003.10.002.
43. Thomas J.D., O'Neill T.M., Dominguez H.D. Perinatal choline supplementation does not mitigate motor coordination deficits associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 2004, 26:223-229. 10.1016/j.ntt.2003.10.005.
44. Ryan S.H., Williams J.K., Thomas J.D. Choline supplementation attenuates learning deficits associated with neonatal alcohol exposure in the rat: effects of varying the timing of choline administration. Brain Res 2008, 1237:91-100. 10.1016/j.brainres.2008.08.048.
45. Thomas J.D., Abou E.J., Dominguez H.D. Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats. Neurotoxicol Teratol 2009, 31:303-311. 10.1016/j.ntt.2009.07.002.
46. Monk B.R., Leslie F.M., Thomas J.D. The effects of perinatal choline supplementation on hippocampal cholinergic development in rats exposed to alcohol during the brain growth spurt. Hippocampus 2012, 22:1750-1757. 10.1002/hipo.22009.
47. Summers B.L., Henry C.M., Rofe A.M., Coyle P. Dietary zinc supplementation during pregnancy prevents spatial and object recognition memory impairments caused by early prenatal ethanol exposure. Behav Brain Res 2008, 186:230-238. 10.1016/j.bbr.2007.08.011.
48. Wainwright P.E., Huang Y.S., Mills D.E., Ward G.R., Ward R.P., McCutcheon D. Interactive effects of prenatal ethanol and N-3 fatty acid supplementation on brain development in mice. Lipids 1989, 24:989-997.
49. Wainwright P.E., Huang Y.S., Simmons V., Mills D.E., Ward R.P., Ward G.R., et al. Effects of prenatal ethanol and long-chain n-3 fatty acid supplementation on development in mice. 2. Fatty acid composition of brain membrane phospholipids. Alcohol Clin Exp Res 1990, 14:413-420.
50. Wainwright P.E., Ward G.R., Winfield D., Huang Y.S., Mills D.E., Ward R.P., et al. Effects of prenatal ethanol and long-chain n-3 fatty acid supplementation on development in mice. 1. Body and brain growth, sensorimotor development, and water T-maze reversal learning. Alcohol Clin Exp Res 1990, 14:405-412.
51. Furuya H., Aikawa H., Yoshida T., Okazaki I. The use of docosahexaenoic acid supplementation to ameliorate the hyperactivity of rat pups induced by in utero ethanol exposure. Environ Health Prev Med 2000, 5:103-110. 10.1265/ehpm.2000.103.
52. Patten A.R., Sickmann H.M., Dyer R.A., Innis S.M., Christie B.R. Omega-3 fatty acids can reverse the long-term deficits in hippocampal synaptic plasticity caused by prenatal ethanol exposure. Neurosci Lett 2013, 10.1016/j.neulet.2013.05.051.
53. Patten A.R., Brocardo P.S., Christie B.R. Omega-3 supplementation can restore glutathione levels and prevent oxidative damage caused by prenatal ethanol exposure. J Nutr Biochem 2013, 24:760-769. 10.1016/j.jnutbio.2012.04.003.
54. Burdge G.C., Postle A.D. Effect of maternal ethanol consumption during pregnancy on the phospholipid molecular species composition of fetal guinea-pig brain, liver and plasma. Biochim Biophys Acta 1995, 1256:346-352.
55. Wen Z., Kim H.Y. Alterations in hippocampal phospholipid profile by prenatal exposure to ethanol. J Neurochem 2004, 89:1368-1377. 10.1111/j.1471-4159.2004.02433.x.
56. Levant B., Ozias M.K., Jones K.A., Carlson S.E. Differential effects of modulation of docosahexaenoic acid content during development in specific regions of rat brain. Lipids 2006, 41:407-414.
57. Miller M.W. Circadian rhythm of cell proliferation in the telencephalic ventricular zone: effect of in utero exposure to ethanol. Brain Res 1992, 595:17-24.
58. Youngentob S.L., Kent P.F., Sheehe P.R., Molina J.C., Spear N.E., Youngentob L.M. Experience-induced fetal plasticity: the effect of gestational ethanol exposure on the behavioral and neurophysiologic olfactory response to ethanol odor in early postnatal and adult rats. Behav Neurosci 2007, 121:1293-1305. 10.1037/0735-7044.121.6.1293.
59. West J.R., Hamre K.M., Pierce D.R. Delay in brain growth induced by alcohol in artificially reared rat pups. Alcohol 1984, 1:213-222.
60. Varlinskaya E.I., Spear L.P., Spear N.E. Social behavior and social motivation in adolescent rats: role of housing conditions and partner's activity. Physiol Behav 1999, 67:475-482.
61. Mooney S.M., Varlinskaya E.I. Acute prenatal exposure to ethanol and social behavior: effects of age, sex, and timing of exposure. Behav Brain Res 2011, 216:358-364. 10.1016/j.bbr.2010.08.014.
62. Middleton F.A., Varlinskaya E.I., Mooney S.M. Molecular substrates of social avoidance seen following prenatal ethanol exposure and its reversal by social enrichment. Dev Neurosci 2012, 34:115-128. 10.1159/000337858.
63. Cohen O.S., Varlinskaya E.I., Wilson C.A., Glatt S.J., Mooney S.M. Acute prenatal exposure to a moderate dose of valproic acid increases social behavior and alters gene expression in rats. Int J Dev Neurosci 2013, 31:740-750. 10.1016/j.ijdevneu.2013.09.002.
64. Varlinskaya E.I., Mooney S.M. Acute exposure to ethanol on gestational day 15 affects social motivation of female offspring. Behav Brain Res 2014, 261:106-109. 10.1016/j.bbr.2013.12.016.
65. Lee L.J., Chen W.J., Chuang Y.W., Wang Y.C. Neonatal whisker trimming causes long-lasting changes in structure and function of the somatosensory system. Exp Neurol 2009, 219:524-532. 10.1016/j.expneurol.2009.07.012.
66. Jirikowic T.L., McCoy S.W., Lubetzky-Vilnai A., Price R., Ciol M.A., Kartin D., et al. Sensory control of balance: a comparison of children with fetal alcohol spectrum disorders to children with typical development. J Popul Ther Clin Pharmacol 2013, 20:e212-e228.
67. Williams L., Jackson C.P., Choe N., Pelland L., Scott S.H., Reynolds J.N. Sensory-motor deficits in children with fetal alcohol spectrum disorder assessed using a robotic virtual reality platform. Alcohol Clin Exp Res 2014, 38:116-125. 10.1111/acer.12225.
68. Hutson K.A., Masterton R.B. The sensory contribution of a single vibrissa's cortical barrel. J Neurophysiol 1986, 56:1196-1223.
69. Harris J.A., Petersen R.S., Diamond M.E. Distribution of tactile learning and its neural basis. Proc Natl Acad Sci U S A 1999, 96:7587-7591.
70. Kehoe P., Shoemaker W. Opioid-dependent behaviors in infant rats: effects of prenatal exposure to ethanol. Pharmacol Biochem Behav 1991, 39:389-394.
71. Lehotzky K., Ungvary G., Szeberenyi J.M., Kiss A. Development of the central nervous system functions in rat pups prenatally exposed to alcohol (study on the behavioural teratology of ethanol in CFY rat pups). Acta Physiol Hung 1988, 72:171-180.
72. Gibson M.A., Butters N.S., Reynolds J.N., Brien J.F. Effects of chronic prenatal ethanol exposure on locomotor activity, and hippocampal weight, neurons, and nitric oxide synthase activity of the young postnatal guinea pig. Neurotoxicol Teratol 2000, 22:183-192.
73. Becker H.C., Randall C.L. Effects of prenatal ethanol exposure in C57BL mice on locomotor activity and passive avoidance behavior. Psychopharmacology (Berl) 1989, 97:40-44.
74. Hamilton D.A., Candelaria-Cook F.T., Akers K.G., Rice J.P., Maes L.I., Rosenberg M., et al. Patterns of social-experience-related c-fos and Arc expression in the frontal cortices of rats exposed to saccharin or moderate levels of ethanol during prenatal brain development. Behav Brain Res 2010, 214:66-74. 10.1016/j.bbr.2010.05.048.
75. Wellmann K.A., Mooney S.M. Unilateral whisker clipping exacerbates ethanol-induced social and somatosensory behavioral deficits in a sex- and age-dependent manner. Physiol Behav 2014, pii:S0031-9384(14)00463-6.
76. Cullen C.L., Burne T.H., Lavidis N.A., Moritz K.M. Low dose prenatal ethanol exposure induces anxiety-like behaviour and alters dendritic morphology in the basolateral amygdala of rat offspring. PLOS ONE 2013, 8:e54924. 10.1371/journal.pone.0054924.
77. Ohta K., Sakata-Haga H., Fukui Y. Alteration in anxiety-related behaviors and reduction of serotonergic neurons in raphe nuclei in adult rats prenatally exposed to ethanol. Congenit Anom (Kyoto) 2010, 50:105-114. 10.1111/j. 1741-4520.2010.00269.x.
78. Ohta K., Sakata-Haga H., Fukui Y. Prenatal ethanol exposure impairs passive avoidance acquisition and enhances unconditioned freezing in rat offspring. Behav Brain Res 2012, 234:255-258. 10.1016/j.bbr.2012.07.001.
79. Sliwowska J.H., Song H.J., Bodnar T., Weinberg J. Prenatal alcohol exposure results in long-term serotonin neuron deficits in female rats: modulatory role of ovarian steroids. Alcohol Clin Exp Res 2014, 38:152-160. 10.1111/acer.12224.
80. Osborn J.A., Kim C.K., Steiger J., Weinberg J. Prenatal ethanol exposure differentially alters behavior in males and females on the elevated plus maze. Alcohol Clin Exp Res 1998, 22:685-696. 10.1097/00000374-199805000-00021.
81. Pellow S., Chopin P., File S.E., Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985, 14:149-167. 10.1016/0165-0270(85)90031-7.
82. Pellow S., File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 1986, 24:525-529. 10.1016/0091-3057(86)90552-6.
83. Hogg S. A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Biochem Behav 1996, 54:21-30. 10.1016/0091-3057(95)02126-4.
84. Hamilton D.A., Barto D., Rodriguez C.I., Magcalas C.M., Fink B.C., Rice J.P., et al. Effects of moderate prenatal ethanol exposure and age on social behavior, spatial response perseveration errors and motor behavior. Behav Brain Res 2014, 269:44-54. 10.1016/j.bbr.2014.04.029.
85. Zimmerberg B., Drucker P.C., Weider J.M. Differential behavioral effects of the neuroactive steroid allopregnanolone on neonatal rats prenatally exposed to alcohol. Pharmacol Biochem Behav 1995, 51:463-468. 10.1016/0091-3057(95)00008-K.
86. Marino M.D., Cronise K., Lugo J.N., Kelly S.J. Ultrasonic vocalizations and maternal-infant interactions in a rat model of fetal alcohol syndrome. Dev Psychobiol 2002, 41:341-351. 10.1002/dev.10077.
87. Rubin M.A., Wellmann K.A., Lewis B., Overgaauw B.J., Littleton J.M., Barron S. Difluoromethylornithine (DFMO) reduces deficits in isolation-induced ultrasonic vocalizations and balance following neonatal ethanol exposure in rats. Pharmacol Biochem Behav 2009, 92:44-50. 10.1016/j.pbb.2008.10.008.
88. Wellmann K., Lewis B., Barron S. Agmatine reduces ultrasonic vocalization deficits in female rat pups exposed neonatally to ethanol. Neurotoxicol Teratol 2010, 32:158-163. 10.1016/j.ntt.2009.11.005.
89. Hofer M.A., Shair H. Ultrasonic vocalization during social interaction and isolation in 2-week-old rats. Dev Psychobiol 1978, 11:495-504. 10.1002/dev.420110513.
90. Noirot E. Ultrasounds and maternal behavior in small rodents. Dev Psychobiol 1972, 5:371-387. 10.1002/dev.420050410.
91. Allin J.T., Banks E.M. Functional aspects of ultrasound production by infant albino rats (Rattus norvegicus). Anim Behav 1972, 20:175-185.
92. Brouette-Lahlou I., Vernet-Maury E., Vigouroux M. Role of pups' ultrasonic calls in a particular maternal behavior in Wistar rat: pups' anogenital licking. Behav Brain Res 1992, 50:147-154.
93. van Hasselt F.N., Tieskens J.M., Trezza V., Krugers H.J., Vanderschuren L.J., Joels M. Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats. Physiol Behav 2012, 106:701-706. 10.1016/j.physbeh.2011.12.007.
94. Edelmann M.N., Demers C.H., Auger A.P. Maternal touch moderates sex differences in juvenile social play behavior. PLOS ONE 2013, 8:e57396. 10.1371/journal.pone.0057396.
95. Portfors C.V. Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci 2007, 46:28-34.
96. Willey A.R., Spear L.P. Effects of ethanol on social approach and 50kHz ultrasonic vocalization production in adolescent male Sprague-Dawley rats. Dev Psychobiol 2014, 56:857-863. 10.1002/dev.21143.
97. Kim H.Y., Akbar M., Lau A., Edsall L. Inhibition of neuronal apoptosis by docosahexaenoic acid (22:6n-3). Role of phosphatidylserine in antiapoptotic effect. J Biol Chem 2000, 275:35215-35223. 10.1074/jbc.M004446200.
98. Akbar M., Kim H.Y. Protective effects of docosahexaenoic acid in staurosporine-induced apoptosis: involvement of phosphatidylinositol-3 kinase pathway. J Neurochem 2002, 82:655-665.
99. Akbar M., Calderon F., Wen Z., Kim H.Y. Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival. Proc Natl Acad Sci U S A 2005, 102:10858-10863. 10.1073/pnas.0502903102.
100. Kim H.Y., Moon H.S., Cao D., Lee J., Kevala K., Jun S.B., et al. N-docosahexaenoylethanolamide promotes development of hippocampal neurons. Biochem J 2011, 435:327-336. 10.1042/BJ20102118.
101. Martin R.E., Bazan N.G. Changing fatty acid content of growth cone lipids prior to synaptogenesis. J Neurochem 1992, 59:318-325.
102. Miller R.R., Ugolini A.M., Nothdorf R.A., Searcy K.J., Taylor C.L., Spidle D.L. Ethanol alters brain phospholipid levels which correlate with altered brain morphology. Comp Biochem Physiol B Biochem Mol Biol 1997, 116:407-417.
103. Kim H.Y. Biochemical and biological functions of docosahexaenoic acid in the nervous system: modulation by ethanol. Chem Phys Lipids 2008, 153:34-46. 10.1016/j.chemphyslip.2008.02.014.
104. Hitzemann R. Developmental changes in the fatty acids of synaptic membrane phospholipids: effect of protein malnutrition. Neurochem Res 1981, 6:935-947.
105. Rice D., Barone S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 2000, 108(Suppl. 3):511-533.
106. Guesnet P., Alessandri J.M. Docosahexaenoic acid (DHA) and the developing central nervous system (CNS) - implications for dietary recommendations. Biochimie 2011, 93:7-12. 10.1016/j.biochi.2010.05.005.