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Published in: Behavioral and Brain Functions 1/2013

Open Access 01-12-2013 | Research

Long-term ω-3 fatty acid supplementation induces anti-stress effects and improves learning in rats

Authors: Miguel Á Pérez, Gonzalo Terreros, Alexies Dagnino-Subiabre

Published in: Behavioral and Brain Functions | Issue 1/2013

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Abstract

Chronic stress leads to secretion of the adrenal steroid hormone corticosterone, inducing hippocampal atrophy and dendritic hypertrophy in the rat amygdala. Both alterations have been correlated with memory impairment and increased anxiety. Supplementation with ω-3 fatty acids improves memory and learning in rats. The aim of this study was to evaluate the effects of ω-3 supplementation on learning and major biological and behavioral stress markers. Male Sprague–Dawley rats were randomly assigned to three experimental groups: 1) Control, 2) Vehicle, animals supplemented with water, and 3) ω-3, rats supplemented with ω-3 (100 mg of DHA+25 mg of EPA). Each experimental group was divided into two subgroups: one of which was not subjected to stress while the other was subjected to a restraint stress paradigm. Afterwards, learning was analyzed by avoidance conditioning. As well, plasma corticosterone levels and anxiety were evaluated as stress markers, respectively by ELISA and the plus-maze test. Restraint stress impaired learning and increased both corticosterone levels and the number of entries into the open-arm (elevated plus-maze). These alterations were prevented by ω-3 supplementation. Thus, our results demonstrate that ω-3 supplementation had two beneficial effects on the stressed rats, a strong anti-stress effect and improved learning.
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Literature
1.
go back to reference Selye H: A syndrome produced by diverse nocuos agents. Nature. 1936, 138 (32): 32-CrossRef Selye H: A syndrome produced by diverse nocuos agents. Nature. 1936, 138 (32): 32-CrossRef
2.
go back to reference Goldstein D, McEwen B: Allostasis, homeostat, and nature of stress. Stress. 2002, 5 (1): 55-58. 10.1080/102538902900012345.CrossRefPubMed Goldstein D, McEwen B: Allostasis, homeostat, and nature of stress. Stress. 2002, 5 (1): 55-58. 10.1080/102538902900012345.CrossRefPubMed
3.
go back to reference Herman JP, Prewitt CM, Cullinan WE: Neuronal circuit regulation of the hypothalamo-pituitary-adrenocortical stress axis. Crit Rev Neurobiol. 1996, 10: 371-394. 10.1615/CritRevNeurobiol.v10.i3-4.50.CrossRefPubMed Herman JP, Prewitt CM, Cullinan WE: Neuronal circuit regulation of the hypothalamo-pituitary-adrenocortical stress axis. Crit Rev Neurobiol. 1996, 10: 371-394. 10.1615/CritRevNeurobiol.v10.i3-4.50.CrossRefPubMed
4.
go back to reference Smith SM, Vale WW: The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci. 2006, 8: 383-395.PubMedCentralPubMed Smith SM, Vale WW: The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci. 2006, 8: 383-395.PubMedCentralPubMed
5.
go back to reference McEwen BS: Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007, 87: 873-904. 10.1152/physrev.00041.2006.CrossRefPubMed McEwen BS: Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007, 87: 873-904. 10.1152/physrev.00041.2006.CrossRefPubMed
6.
go back to reference O’Connor TM, O’Halloran DJ, Shanahan F: The stress response and the hyphotalamic-pituitary-adrenal axis: from molecule to melancholia. Q J Med. 2000, 93: 323-333. 10.1093/qjmed/93.6.323.CrossRef O’Connor TM, O’Halloran DJ, Shanahan F: The stress response and the hyphotalamic-pituitary-adrenal axis: from molecule to melancholia. Q J Med. 2000, 93: 323-333. 10.1093/qjmed/93.6.323.CrossRef
7.
go back to reference Reul JM, de Kloet ER: Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology. 1985, 117: 2505-2511. 10.1210/endo-117-6-2505.CrossRefPubMed Reul JM, de Kloet ER: Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology. 1985, 117: 2505-2511. 10.1210/endo-117-6-2505.CrossRefPubMed
8.
go back to reference Gray TS, Bingaman EW: The amygdala: Corticotropin-releasing factor, steroids, and stress. Crit Rev Neurobiol. 1996, 10: 155-168. 10.1615/CritRevNeurobiol.v10.i2.10.CrossRefPubMed Gray TS, Bingaman EW: The amygdala: Corticotropin-releasing factor, steroids, and stress. Crit Rev Neurobiol. 1996, 10: 155-168. 10.1615/CritRevNeurobiol.v10.i2.10.CrossRefPubMed
9.
go back to reference Joels M: Corticosteroid actions in the hippocampus. J Neuroendocrinol. 2001, 13: 657-669. 10.1046/j.1365-2826.2001.00688.x.CrossRefPubMed Joels M: Corticosteroid actions in the hippocampus. J Neuroendocrinol. 2001, 13: 657-669. 10.1046/j.1365-2826.2001.00688.x.CrossRefPubMed
10.
go back to reference Wellman CL: Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol. 2001, 49: 245-253. 10.1002/neu.1079.CrossRefPubMed Wellman CL: Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol. 2001, 49: 245-253. 10.1002/neu.1079.CrossRefPubMed
11.
go back to reference McEwen BS: Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus. 1992, 2: 431-436. 10.1002/hipo.450020410.CrossRefPubMed McEwen BS: Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus. 1992, 2: 431-436. 10.1002/hipo.450020410.CrossRefPubMed
12.
go back to reference Watanabe Y, Gould E, Cameron HA, Daniels DC, McEwen BS: Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus. 1992, 2: 431-435. 10.1002/hipo.450020410.CrossRefPubMed Watanabe Y, Gould E, Cameron HA, Daniels DC, McEwen BS: Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus. 1992, 2: 431-435. 10.1002/hipo.450020410.CrossRefPubMed
13.
go back to reference Magariños AM, Orchinik M, McEwen BS: Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: a paradox. Brain Res. 1998, 809: 314-8. 10.1016/S0006-8993(98)00882-8.CrossRefPubMed Magariños AM, Orchinik M, McEwen BS: Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: a paradox. Brain Res. 1998, 809: 314-8. 10.1016/S0006-8993(98)00882-8.CrossRefPubMed
14.
go back to reference Cordero MI, Merino JJ, Sandi C: Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. Behav Neurosci. 2008, 112 (4): 885-91.CrossRef Cordero MI, Merino JJ, Sandi C: Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. Behav Neurosci. 2008, 112 (4): 885-91.CrossRef
15.
go back to reference Conrad CD, McMillan DD, Tsekhanov S, Wright RL, Baran SE, Fuchs RE: Influence of chronic corticosterone and glucocorticoid receptor antagonism in the amygdala on fear conditioning. Neurobiol Learn Mem. 2004, 81: 185-199. 10.1016/j.nlm.2004.01.002.CrossRefPubMed Conrad CD, McMillan DD, Tsekhanov S, Wright RL, Baran SE, Fuchs RE: Influence of chronic corticosterone and glucocorticoid receptor antagonism in the amygdala on fear conditioning. Neurobiol Learn Mem. 2004, 81: 185-199. 10.1016/j.nlm.2004.01.002.CrossRefPubMed
16.
go back to reference Mitra R, Sapolsky RM: Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc Natl Acad Sci. 2008, 105: 5573-8. 10.1073/pnas.0705615105.PubMedCentralCrossRefPubMed Mitra R, Sapolsky RM: Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc Natl Acad Sci. 2008, 105: 5573-8. 10.1073/pnas.0705615105.PubMedCentralCrossRefPubMed
17.
go back to reference Magariños AM, McEwen BS, Flugge G, Fuchs E: Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci. 1996, 16: 3534-3540.PubMed Magariños AM, McEwen BS, Flugge G, Fuchs E: Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci. 1996, 16: 3534-3540.PubMed
18.
go back to reference Vyas S, Béchade C, Riveau B, Downward J, Triller A: Involvement of survival motor neuron (SMN) protein in cell death. Hum Mol Gen. 2002, 11: 2751-2764. 10.1093/hmg/11.22.2751.CrossRefPubMed Vyas S, Béchade C, Riveau B, Downward J, Triller A: Involvement of survival motor neuron (SMN) protein in cell death. Hum Mol Gen. 2002, 11: 2751-2764. 10.1093/hmg/11.22.2751.CrossRefPubMed
19.
go back to reference Dagnino-Subiabre A, Pérez MÁ, Terreros G, Cheng MY, House P, Sapolsky R: Corticosterone treatment impairs auditory fear learning and the dendritic morphology of the rat inferior colliculus. Hear Res. 2012, 294 (1–2): 104-13.CrossRefPubMed Dagnino-Subiabre A, Pérez MÁ, Terreros G, Cheng MY, House P, Sapolsky R: Corticosterone treatment impairs auditory fear learning and the dendritic morphology of the rat inferior colliculus. Hear Res. 2012, 294 (1–2): 104-13.CrossRefPubMed
20.
go back to reference Luine V, Villegas M, Martinez C, McEwen BS: Repeated stress causes reversible impairments of spatial memory performance. Short communication Brain Res. 1994, 639: 167-170. 10.1016/0006-8993(94)91778-7.CrossRef Luine V, Villegas M, Martinez C, McEwen BS: Repeated stress causes reversible impairments of spatial memory performance. Short communication Brain Res. 1994, 639: 167-170. 10.1016/0006-8993(94)91778-7.CrossRef
21.
go back to reference Magariños AM, McEwen BS: Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neurosci. 1995, 69: 89-98. 10.1016/0306-4522(95)00259-L.CrossRef Magariños AM, McEwen BS: Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neurosci. 1995, 69: 89-98. 10.1016/0306-4522(95)00259-L.CrossRef
22.
go back to reference McEwen BS, Chattarji S: Molecular mechanisms of neuroplasticity and pharmacological implications: the example of tianeptine. Eur Neuropsychopharm. 2004, 14 (Suppl. 5): 497-502.CrossRef McEwen BS, Chattarji S: Molecular mechanisms of neuroplasticity and pharmacological implications: the example of tianeptine. Eur Neuropsychopharm. 2004, 14 (Suppl. 5): 497-502.CrossRef
23.
go back to reference Ohl F, Arndt SS, Van der Staay FJ: Pathological anxiety in animals. Vet J. 2008, 175 (1): 18-26. 10.1016/j.tvjl.2006.12.013.CrossRefPubMed Ohl F, Arndt SS, Van der Staay FJ: Pathological anxiety in animals. Vet J. 2008, 175 (1): 18-26. 10.1016/j.tvjl.2006.12.013.CrossRefPubMed
24.
go back to reference Pruessner JC, Baldwin MW, Dedovic K, Renwick R, Mahani NJ, Lord C, Meaney M, Lupien S: Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. Neuroimage. 2005, 28: 815-826. 10.1016/j.neuroimage.2005.06.014.CrossRefPubMed Pruessner JC, Baldwin MW, Dedovic K, Renwick R, Mahani NJ, Lord C, Meaney M, Lupien S: Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. Neuroimage. 2005, 28: 815-826. 10.1016/j.neuroimage.2005.06.014.CrossRefPubMed
25.
go back to reference Liston C, McEwen BS, Casey BJ: Psychosocial stress reversibly disrupts prefrontal processing and attentional control. PNAS. 2009, 106 (3): 912-917. 10.1073/pnas.0807041106.PubMedCentralCrossRefPubMed Liston C, McEwen BS, Casey BJ: Psychosocial stress reversibly disrupts prefrontal processing and attentional control. PNAS. 2009, 106 (3): 912-917. 10.1073/pnas.0807041106.PubMedCentralCrossRefPubMed
26.
go back to reference Choi JS, Christopher K, Kim JJ: The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats. Learn Mem. 2010, 17: 139-147. 10.1101/lm.1676610.PubMedCentralCrossRefPubMed Choi JS, Christopher K, Kim JJ: The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats. Learn Mem. 2010, 17: 139-147. 10.1101/lm.1676610.PubMedCentralCrossRefPubMed
27.
go back to reference Dagnino-Subiabre A, Terreros G, Carmona-Fontaine C, Zepeda R, Orellana JA, Díaz-Véliz G, Mora S, Aboitiz F: Chronic stress impairs acoustic conditioning more than visual conditioning in rats: morphological and behavioural evidence. Neurosci. 2005, 135 (4): 1067-1074. 10.1016/j.neuroscience.2005.07.032.CrossRef Dagnino-Subiabre A, Terreros G, Carmona-Fontaine C, Zepeda R, Orellana JA, Díaz-Véliz G, Mora S, Aboitiz F: Chronic stress impairs acoustic conditioning more than visual conditioning in rats: morphological and behavioural evidence. Neurosci. 2005, 135 (4): 1067-1074. 10.1016/j.neuroscience.2005.07.032.CrossRef
28.
go back to reference Dagnino-Subiabre A: Effects of chronic stress on the auditory system and fear learning: an evolutionary approach. Rev Neurosci. 2013, 18: 1-11. Dagnino-Subiabre A: Effects of chronic stress on the auditory system and fear learning: an evolutionary approach. Rev Neurosci. 2013, 18: 1-11.
29.
go back to reference Baran SE, Armstrong CE, Niren DC, Hanna JJ, Conrad CD: Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiol Learn Mem. 2005, 91: 323-332.CrossRef Baran SE, Armstrong CE, Niren DC, Hanna JJ, Conrad CD: Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiol Learn Mem. 2005, 91: 323-332.CrossRef
30.
go back to reference Takeuchi T, Iwanaga M, Harada E: Possible regulatory mechanism of DHA-induced anti-stress reaction in rats. Brain Res. 2003, 964: 136-143. 10.1016/S0006-8993(02)04113-6.CrossRefPubMed Takeuchi T, Iwanaga M, Harada E: Possible regulatory mechanism of DHA-induced anti-stress reaction in rats. Brain Res. 2003, 964: 136-143. 10.1016/S0006-8993(02)04113-6.CrossRefPubMed
31.
go back to reference Mathieu G, Oualian C, Denis I, Lavialle M, Gisquet-Verrier P, Vancassel S: Dietary n-3 polyunsaturated fatty acid deprivation together with early maternal separation increases anxiety and vulnerability to stress in adult rats. Prostag Leukot Essent Fatty Acids. 2011, 85 (3–4): 129-36.CrossRef Mathieu G, Oualian C, Denis I, Lavialle M, Gisquet-Verrier P, Vancassel S: Dietary n-3 polyunsaturated fatty acid deprivation together with early maternal separation increases anxiety and vulnerability to stress in adult rats. Prostag Leukot Essent Fatty Acids. 2011, 85 (3–4): 129-36.CrossRef
32.
go back to reference Buydens-Branchey L, Branchey M, Hibbeln JR: n-3 Polyunsaturated fatty acids decrease anxiety feelings in a population of substance abusers. J Clin Psycho-pharmacol. 2008, 26 (6): 660-665. Buydens-Branchey L, Branchey M, Hibbeln JR: n-3 Polyunsaturated fatty acids decrease anxiety feelings in a population of substance abusers. J Clin Psycho-pharmacol. 2008, 26 (6): 660-665.
33.
go back to reference Ferraz AC, Kiss A, Araujo RL, Salles HM, Naliwaiko K, Pamplona J: The antidepressant role of dietary long-chain polyunsaturated n-3 fatty acids in two phases in the developing brain. Prostag Leukotr Essent Fatty Acids. 2008, 78: 183-188. 10.1016/j.plefa.2008.02.001.CrossRef Ferraz AC, Kiss A, Araujo RL, Salles HM, Naliwaiko K, Pamplona J: The antidepressant role of dietary long-chain polyunsaturated n-3 fatty acids in two phases in the developing brain. Prostag Leukotr Essent Fatty Acids. 2008, 78: 183-188. 10.1016/j.plefa.2008.02.001.CrossRef
34.
go back to reference du Bois TM, Deng C, Huang XF: Membrane phospholipid composition, alterations in neurotransmitter systems and schizophrenia. Prog Neuro-Psychoph. 2005, 29: 878-888. 10.1016/j.pnpbp.2005.04.034.CrossRef du Bois TM, Deng C, Huang XF: Membrane phospholipid composition, alterations in neurotransmitter systems and schizophrenia. Prog Neuro-Psychoph. 2005, 29: 878-888. 10.1016/j.pnpbp.2005.04.034.CrossRef
35.
go back to reference Calon F, Cole G: Neuroprotective action of omega-3 polyunsaturated fatty acids against neurodegene rative diseases: Evidence from animal studies. Prostag Leukotr Ess. 2007, 7: 287-293.CrossRef Calon F, Cole G: Neuroprotective action of omega-3 polyunsaturated fatty acids against neurodegene rative diseases: Evidence from animal studies. Prostag Leukotr Ess. 2007, 7: 287-293.CrossRef
36.
go back to reference Sinn N, Bryan J, Wilson C: Cognitive effects of polyunsaturated fatty acids in children with attention deficit hyperactivity disorder symptoms: a randomised controlled trial. Prostag Leukotr Essent Fatty Acids. 2008, 78: 311-326. 10.1016/j.plefa.2008.04.004.CrossRef Sinn N, Bryan J, Wilson C: Cognitive effects of polyunsaturated fatty acids in children with attention deficit hyperactivity disorder symptoms: a randomised controlled trial. Prostag Leukotr Essent Fatty Acids. 2008, 78: 311-326. 10.1016/j.plefa.2008.04.004.CrossRef
37.
go back to reference Colangeno LA, He MS, Whooley MA, Daviglus ML, Liu K: Higher dietarty intake of long-chain ω-3 polyunsaturated fatty acids is inversely associated with depressive symtoms in women. Nutrition. 2009, 25: 1011-1119. 10.1016/j.nut.2008.12.008.CrossRef Colangeno LA, He MS, Whooley MA, Daviglus ML, Liu K: Higher dietarty intake of long-chain ω-3 polyunsaturated fatty acids is inversely associated with depressive symtoms in women. Nutrition. 2009, 25: 1011-1119. 10.1016/j.nut.2008.12.008.CrossRef
38.
go back to reference Bourre JM, Francois M, Youyou A, Dumont O, Piciotti M, Pascal G, Dumont G: The effects of dietary α-Linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. Lipids. 1989, 119: 1880-1892. Bourre JM, Francois M, Youyou A, Dumont O, Piciotti M, Pascal G, Dumont G: The effects of dietary α-Linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. Lipids. 1989, 119: 1880-1892.
39.
go back to reference De Vriese SR, Christophe AB, Maes M: Lowered serum n-3 polyunsaturated fatty acid (PUFA) levels predict the occurrence of postpartum depression: further evidence that lowered n-PUFAs are related to major depression. Life Sci. 2003, 73 (25): 3181-3187. 10.1016/j.lfs.2003.02.001.CrossRefPubMed De Vriese SR, Christophe AB, Maes M: Lowered serum n-3 polyunsaturated fatty acid (PUFA) levels predict the occurrence of postpartum depression: further evidence that lowered n-PUFAs are related to major depression. Life Sci. 2003, 73 (25): 3181-3187. 10.1016/j.lfs.2003.02.001.CrossRefPubMed
40.
go back to reference Ross BM: Omega-3 polyunsaturated fatty acids and anxiety disorders. Prostag Leukotr Ess Fatty Acids. 2009, 81: 309-312. 10.1016/j.plefa.2009.10.004.CrossRef Ross BM: Omega-3 polyunsaturated fatty acids and anxiety disorders. Prostag Leukotr Ess Fatty Acids. 2009, 81: 309-312. 10.1016/j.plefa.2009.10.004.CrossRef
41.
go back to reference Su KP: Mind-body interface: the role of n-3 fatty acids in psychoneuroimmunology, somatic presentation, and medical illness comorbidity of depression. Asia Pac J Clin Nutr. 2008, 17: 151-157.PubMed Su KP: Mind-body interface: the role of n-3 fatty acids in psychoneuroimmunology, somatic presentation, and medical illness comorbidity of depression. Asia Pac J Clin Nutr. 2008, 17: 151-157.PubMed
42.
go back to reference Tafet GE, Bernardini R: Psychoneuroendocrinological links between chronic stress and depression. Prog Neuropsychopharmacol Biol Psychiatry. 2003, 27 (6): 893-903. 10.1016/S0278-5846(03)00162-3.CrossRefPubMed Tafet GE, Bernardini R: Psychoneuroendocrinological links between chronic stress and depression. Prog Neuropsychopharmacol Biol Psychiatry. 2003, 27 (6): 893-903. 10.1016/S0278-5846(03)00162-3.CrossRefPubMed
43.
go back to reference McFadden LM, Paris JJ, Mitzelfelt MS, McDonough S, Frye CA, Matuszewich L: Sex-dependent effects of chronic unpredictable stress in the water maze. Physiol Behav. 2011, 102 (3–4): 266-75.CrossRefPubMed McFadden LM, Paris JJ, Mitzelfelt MS, McDonough S, Frye CA, Matuszewich L: Sex-dependent effects of chronic unpredictable stress in the water maze. Physiol Behav. 2011, 102 (3–4): 266-75.CrossRefPubMed
44.
go back to reference Riemer S, Maes M, Christophe A, Rief W: Lowered omega-3 PUFAs are related to major depression, but not to somatization syndrome. J Affective Disorders. 2010, 123 (3): 173-180.CrossRef Riemer S, Maes M, Christophe A, Rief W: Lowered omega-3 PUFAs are related to major depression, but not to somatization syndrome. J Affective Disorders. 2010, 123 (3): 173-180.CrossRef
45.
go back to reference Kleen J, Sitomer M, Killeen P, Conrad CD: Chronic stress impairs spatial memory and motivation for reward without disrupting motor ability and motivation to explore. Behav Neurosci. 2006, In press Kleen J, Sitomer M, Killeen P, Conrad CD: Chronic stress impairs spatial memory and motivation for reward without disrupting motor ability and motivation to explore. Behav Neurosci. 2006, In press
46.
go back to reference Watanabe Y, Gould E, McEwen BS: Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 1992, 588: 341-345. 10.1016/0006-8993(92)91597-8.CrossRefPubMed Watanabe Y, Gould E, McEwen BS: Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 1992, 588: 341-345. 10.1016/0006-8993(92)91597-8.CrossRefPubMed
47.
go back to reference Madsen L, Petersen RK, Kristianse K: Regulation of adipocyte differentiation and function by polyunsaturated fatty acids. Biochim Biophys Acta. 2005, 1740: 266-286. 10.1016/j.bbadis.2005.03.001.CrossRefPubMed Madsen L, Petersen RK, Kristianse K: Regulation of adipocyte differentiation and function by polyunsaturated fatty acids. Biochim Biophys Acta. 2005, 1740: 266-286. 10.1016/j.bbadis.2005.03.001.CrossRefPubMed
48.
go back to reference Maffei M, Halaas J, Ravussin E, Pratley RE, Lee LH, Zhang Y, Frei H, Kim S, Lallone R, Ranganathan S: Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med. 1995, 1 (11): 1155-1161. 10.1038/nm1195-1155.CrossRefPubMed Maffei M, Halaas J, Ravussin E, Pratley RE, Lee LH, Zhang Y, Frei H, Kim S, Lallone R, Ranganathan S: Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med. 1995, 1 (11): 1155-1161. 10.1038/nm1195-1155.CrossRefPubMed
49.
go back to reference Stanley S, Wymme K, McGowan Bloom S: Hormonal regulation of food intake. Physiol Rev. 2005, 85: 1131-1158. 10.1152/physrev.00015.2004.CrossRefPubMed Stanley S, Wymme K, McGowan Bloom S: Hormonal regulation of food intake. Physiol Rev. 2005, 85: 1131-1158. 10.1152/physrev.00015.2004.CrossRefPubMed
50.
go back to reference Ferraz AC, Delattre AM, Almendra RG, Sonagli M, Borges C, Araujo P, Andersen ML, Tufik S: Chronic omega-3 fatty acids supplementation promotes beneficial effects on anxiety, cognitive and depressive-like behaviors in rats subjected to a restraint stress protocol. Behav Brain Res. 2011, 219: 116-122. 10.1016/j.bbr.2010.12.028.CrossRefPubMed Ferraz AC, Delattre AM, Almendra RG, Sonagli M, Borges C, Araujo P, Andersen ML, Tufik S: Chronic omega-3 fatty acids supplementation promotes beneficial effects on anxiety, cognitive and depressive-like behaviors in rats subjected to a restraint stress protocol. Behav Brain Res. 2011, 219: 116-122. 10.1016/j.bbr.2010.12.028.CrossRefPubMed
51.
go back to reference Davis M: Are different parts of the extended amygdala involved in fear versus anxiety?. Soc Biol Psy. 1998, 44: 1239-1247. 10.1016/S0006-3223(98)00288-1.CrossRef Davis M: Are different parts of the extended amygdala involved in fear versus anxiety?. Soc Biol Psy. 1998, 44: 1239-1247. 10.1016/S0006-3223(98)00288-1.CrossRef
52.
go back to reference Davis M, Walker DL, Miles L, Grillon C: Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuro-psychophar Rev. 2010, 35: 105-135. Davis M, Walker DL, Miles L, Grillon C: Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuro-psychophar Rev. 2010, 35: 105-135.
53.
go back to reference Pêgo JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OFX, Sousa N: Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur J Neurosci. 2008, 27: 1503-1516. 10.1111/j.1460-9568.2008.06112.x.CrossRefPubMed Pêgo JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OFX, Sousa N: Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur J Neurosci. 2008, 27: 1503-1516. 10.1111/j.1460-9568.2008.06112.x.CrossRefPubMed
54.
go back to reference Vyas A, Bernal S, Chattarji S: Effects of chronic stress on dendritic arborization in the central and extended amygdale. Brain Res. 2003, 965: 290-294. 10.1016/S0006-8993(02)04162-8.CrossRefPubMed Vyas A, Bernal S, Chattarji S: Effects of chronic stress on dendritic arborization in the central and extended amygdale. Brain Res. 2003, 965: 290-294. 10.1016/S0006-8993(02)04162-8.CrossRefPubMed
55.
go back to reference Vyas A, Pillai AG, Chattarji S: Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neurosci. 2004, 128: 667-673. 10.1016/j.neuroscience.2004.07.013.CrossRef Vyas A, Pillai AG, Chattarji S: Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neurosci. 2004, 128: 667-673. 10.1016/j.neuroscience.2004.07.013.CrossRef
56.
go back to reference Guo JD, Rainnie DG: Presynaptic 5-HT(1B) receptor-mediated serotonergic inhibition of glutamate transmission in the bed nucleus of the stria terminalis. Neuroscience. 2010, 165 (4): 1390-401. 10.1016/j.neuroscience.2009.11.071.PubMedCentralCrossRefPubMed Guo JD, Rainnie DG: Presynaptic 5-HT(1B) receptor-mediated serotonergic inhibition of glutamate transmission in the bed nucleus of the stria terminalis. Neuroscience. 2010, 165 (4): 1390-401. 10.1016/j.neuroscience.2009.11.071.PubMedCentralCrossRefPubMed
57.
go back to reference Levita L, Hammack SE, Mania I, Li XY, Davis M, Rainnie DG: 5-hydroxytryptamine1A-like receptor activation in the bed nucleus of the stria terminalis: electrophysiological and behavioral studies. Neuroscience. 2004, 128: 583-596. 10.1016/j.neuroscience.2004.06.037.CrossRefPubMed Levita L, Hammack SE, Mania I, Li XY, Davis M, Rainnie DG: 5-hydroxytryptamine1A-like receptor activation in the bed nucleus of the stria terminalis: electrophysiological and behavioral studies. Neuroscience. 2004, 128: 583-596. 10.1016/j.neuroscience.2004.06.037.CrossRefPubMed
58.
go back to reference Sunanda , Rao BS, Raju TR: Restraint stress-induced alterations in the levels of biogenic amines, amino acids, and AChE activity in the hippocampus. Neurochem Res. 2000, 25 (12): 1547-52. 10.1023/A:1026606201069.CrossRefPubMed Sunanda , Rao BS, Raju TR: Restraint stress-induced alterations in the levels of biogenic amines, amino acids, and AChE activity in the hippocampus. Neurochem Res. 2000, 25 (12): 1547-52. 10.1023/A:1026606201069.CrossRefPubMed
59.
go back to reference Torres IL, Gamaro GD, Vasconcellos AP, Silveira R, Dalmaz C: Effects of chronic restraint stress on feeding behavior and on monoamine levels in different brain structures in rats. Neurochem Res. 2002, 27 (6): 519-25. 10.1023/A:1019856821430.CrossRefPubMed Torres IL, Gamaro GD, Vasconcellos AP, Silveira R, Dalmaz C: Effects of chronic restraint stress on feeding behavior and on monoamine levels in different brain structures in rats. Neurochem Res. 2002, 27 (6): 519-25. 10.1023/A:1019856821430.CrossRefPubMed
60.
go back to reference Vancassel S, Leman S, Hanonick L, Denis S, Roger J, Nollet M, Bodard S, Kousignian I, Belzung C, Chalon S: n-3 Polyunsaturated fatty acid supplementation reverses stress-induced modifications on brain monoamine levels in mice. J Lipid Res. 2008, 49: 340-348.CrossRefPubMed Vancassel S, Leman S, Hanonick L, Denis S, Roger J, Nollet M, Bodard S, Kousignian I, Belzung C, Chalon S: n-3 Polyunsaturated fatty acid supplementation reverses stress-induced modifications on brain monoamine levels in mice. J Lipid Res. 2008, 49: 340-348.CrossRefPubMed
61.
go back to reference Galea LM, McEwen MS, Tanapat P, Deak T, Spencer RL, Dhabhar FS: Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience. 1997, 81: 689-697. 10.1016/S0306-4522(97)00233-9.CrossRefPubMed Galea LM, McEwen MS, Tanapat P, Deak T, Spencer RL, Dhabhar FS: Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience. 1997, 81: 689-697. 10.1016/S0306-4522(97)00233-9.CrossRefPubMed
62.
go back to reference Cook SC, Wellman CL: Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurolbiol. 2004, 60 (2): 236-248. 10.1002/neu.20025.CrossRef Cook SC, Wellman CL: Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurolbiol. 2004, 60 (2): 236-248. 10.1002/neu.20025.CrossRef
63.
go back to reference Gadek-Michalska A, Bugasjki J: Repeated handling, restraint, or chronic crowding impair the hypothalamic-pituitary-adrenocortical response to acute restraint stress. J Physiol Pharmacol. 2003, 54 (3): 449-59.PubMed Gadek-Michalska A, Bugasjki J: Repeated handling, restraint, or chronic crowding impair the hypothalamic-pituitary-adrenocortical response to acute restraint stress. J Physiol Pharmacol. 2003, 54 (3): 449-59.PubMed
64.
go back to reference LeDoux JE, Sakaeuchi A, Reis DJ: Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned by acoustic stimuli. J Neurosci. 1984, 4: 683-698.PubMed LeDoux JE, Sakaeuchi A, Reis DJ: Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned by acoustic stimuli. J Neurosci. 1984, 4: 683-698.PubMed
65.
go back to reference Dagnino-Subiabre A, Muñoz-Llancao P, Terreros G, Wyneken U, Díaz-Véliz G, Porter B, Kilgard MP, Atzori M, Aboitiz F: Chronic stress induces dendritic atrophy in the rat medial geniculate nucleus: effects on auditory conditioning. Behav Brain Res. 2009, 203 (1): 88-96. 10.1016/j.bbr.2009.04.024.CrossRefPubMed Dagnino-Subiabre A, Muñoz-Llancao P, Terreros G, Wyneken U, Díaz-Véliz G, Porter B, Kilgard MP, Atzori M, Aboitiz F: Chronic stress induces dendritic atrophy in the rat medial geniculate nucleus: effects on auditory conditioning. Behav Brain Res. 2009, 203 (1): 88-96. 10.1016/j.bbr.2009.04.024.CrossRefPubMed
66.
go back to reference Bose M, Muñoz-Llancao P, Roychowdhury S, Nichols JA, Jakkamsetti V, Porter B, Byrapureddy R, Salgado H, Kilgard MP, Aboitiz F, Dagnino-Subiabre A, Atzori M: Effect of the environment on the dendritic morphology of the rat auditory cortex. Synapse. 2010, 64 (2): 97-110. 10.1002/syn.20710.PubMedCentralCrossRefPubMed Bose M, Muñoz-Llancao P, Roychowdhury S, Nichols JA, Jakkamsetti V, Porter B, Byrapureddy R, Salgado H, Kilgard MP, Aboitiz F, Dagnino-Subiabre A, Atzori M: Effect of the environment on the dendritic morphology of the rat auditory cortex. Synapse. 2010, 64 (2): 97-110. 10.1002/syn.20710.PubMedCentralCrossRefPubMed
67.
go back to reference Hu M, Yu J, Ma Y, Yang W, Mu D, Kong L, Xiang L, Yang G, Xie P: Prognostic impact of hypoxia imaging with 18f-fluoroerythronitroimidazole with integrated positron emission tomography and computed tomography in non-small cell lung cancer. J Clin Oncol. 2010, 28 (15): Hu M, Yu J, Ma Y, Yang W, Mu D, Kong L, Xiang L, Yang G, Xie P: Prognostic impact of hypoxia imaging with 18f-fluoroerythronitroimidazole with integrated positron emission tomography and computed tomography in non-small cell lung cancer. J Clin Oncol. 2010, 28 (15):
68.
go back to reference Ikemoto A, Ohishi M, Sato Y, Hata N, Misawa Y, Fujii Y, Okuyama H: Reversibility of n-3 fatty acid deficiency-induced alterations of learning behavior in the rat: level of n-6 fatty acids as another critical factor. J Lipid Res. 2001, 42: 1655-1663.PubMed Ikemoto A, Ohishi M, Sato Y, Hata N, Misawa Y, Fujii Y, Okuyama H: Reversibility of n-3 fatty acid deficiency-induced alterations of learning behavior in the rat: level of n-6 fatty acids as another critical factor. J Lipid Res. 2001, 42: 1655-1663.PubMed
69.
go back to reference Obradovic DI, Savic MM, Andjelkovic DA, Ugresic ND, Bokonjic DR: The influence of midazolam on active avoidance retrieval and acquisition rate in rats. Pharmacol Biochem Be. 2004, 77 (1): 77-83. 10.1016/j.pbb.2003.09.018.CrossRef Obradovic DI, Savic MM, Andjelkovic DA, Ugresic ND, Bokonjic DR: The influence of midazolam on active avoidance retrieval and acquisition rate in rats. Pharmacol Biochem Be. 2004, 77 (1): 77-83. 10.1016/j.pbb.2003.09.018.CrossRef
70.
go back to reference McNamara RK, Carlson SE: Role of omega-3 fatty acids in brain development and function: potential implications for the pathogenesis and prevention of psychopathology. Prostaglandins Leukot Essent Fatty Acids. 2006, 75: 329-349. 10.1016/j.plefa.2006.07.010.CrossRefPubMed McNamara RK, Carlson SE: Role of omega-3 fatty acids in brain development and function: potential implications for the pathogenesis and prevention of psychopathology. Prostaglandins Leukot Essent Fatty Acids. 2006, 75: 329-349. 10.1016/j.plefa.2006.07.010.CrossRefPubMed
71.
go back to reference Hennebelle M, Balasse L, Latour A, Champeil-Potokar G, Denis S, Lavialle M, Gisquet-Verrier P, Denis I, Vancassel S: Influence of omega-3 fatty acid status on the way rats adapt to chronic restraint stress. PLoS One. 2012, 7: e42142-10.1371/journal.pone.0042142.PubMedCentralCrossRefPubMed Hennebelle M, Balasse L, Latour A, Champeil-Potokar G, Denis S, Lavialle M, Gisquet-Verrier P, Denis I, Vancassel S: Influence of omega-3 fatty acid status on the way rats adapt to chronic restraint stress. PLoS One. 2012, 7: e42142-10.1371/journal.pone.0042142.PubMedCentralCrossRefPubMed
72.
go back to reference Laugero KD, Smilowitz JT, German JB, Jarcho MR, Mendoza SP, Bales KL: Plasma omega 3 polyunsaturated fatty acid status and monounsaturated fatty acids are altered by chronic social stress and predict endocrine responses to acute stress in titi monkeys. Prostaglandins. Leukot Essent Fatty Acids. 2011, 84 (3–4): 71-8.CrossRef Laugero KD, Smilowitz JT, German JB, Jarcho MR, Mendoza SP, Bales KL: Plasma omega 3 polyunsaturated fatty acid status and monounsaturated fatty acids are altered by chronic social stress and predict endocrine responses to acute stress in titi monkeys. Prostaglandins. Leukot Essent Fatty Acids. 2011, 84 (3–4): 71-8.CrossRef
74.
75.
go back to reference Häring M, Guggenhuber S, Lutz B: Neuronal populations mediating the effects of endocannabinoids on stress and emotionality. Neuroscience. 2012, 204: 145-58.CrossRefPubMed Häring M, Guggenhuber S, Lutz B: Neuronal populations mediating the effects of endocannabinoids on stress and emotionality. Neuroscience. 2012, 204: 145-58.CrossRefPubMed
76.
go back to reference Gross C, Zhuang X, Stark K, Ramboz S, Oosting R, Kirby L, Santarelli L, Beck S, Hen R: Serotonin 1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature. 2002, 416: 396-400. 10.1038/416396a.CrossRefPubMed Gross C, Zhuang X, Stark K, Ramboz S, Oosting R, Kirby L, Santarelli L, Beck S, Hen R: Serotonin 1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature. 2002, 416: 396-400. 10.1038/416396a.CrossRefPubMed
77.
go back to reference Kodas E, Galineau L, Bodard S, Vancassel S, Guilloteau D, Besnard JC, Chalon S: Serotoninergic neurotransmission is affected by n-3 polyunsaturated fatty acids in the rat. J Neurochem. 2004, 89: 695-702. 10.1111/j.1471-4159.2004.02401.x.CrossRefPubMed Kodas E, Galineau L, Bodard S, Vancassel S, Guilloteau D, Besnard JC, Chalon S: Serotoninergic neurotransmission is affected by n-3 polyunsaturated fatty acids in the rat. J Neurochem. 2004, 89: 695-702. 10.1111/j.1471-4159.2004.02401.x.CrossRefPubMed
78.
go back to reference Kiss JZ, Troncoso E, Djebbara Z, Vutskits L, Muller D: The role of neural cell adhesion molecules in plasticity and repair. Brain Res Rev. 2001, 36 (2–3): 175-184.CrossRefPubMed Kiss JZ, Troncoso E, Djebbara Z, Vutskits L, Muller D: The role of neural cell adhesion molecules in plasticity and repair. Brain Res Rev. 2001, 36 (2–3): 175-184.CrossRefPubMed
79.
go back to reference Rumpel S, LeDoux J, Zador A, Malinow R: Postsynaptic receptor trafficking underlying a form of associative learning. Science. 2005, 308: 83-88. 10.1126/science.1103944.CrossRefPubMed Rumpel S, LeDoux J, Zador A, Malinow R: Postsynaptic receptor trafficking underlying a form of associative learning. Science. 2005, 308: 83-88. 10.1126/science.1103944.CrossRefPubMed
80.
go back to reference Venna VR, Deplanque D, Allet C, Belarbi K, Hamdane M, Bordet R: PUFA induce antidepressant-like effects in parallel to structural and molecular changes in the hippocampus. Psychoneuroendocrinology. 2009, 34 (2): 199-211. 10.1016/j.psyneuen.2008.08.025.CrossRefPubMed Venna VR, Deplanque D, Allet C, Belarbi K, Hamdane M, Bordet R: PUFA induce antidepressant-like effects in parallel to structural and molecular changes in the hippocampus. Psychoneuroendocrinology. 2009, 34 (2): 199-211. 10.1016/j.psyneuen.2008.08.025.CrossRefPubMed
81.
go back to reference Laino CH, Fonseca C, Sterin-Speziale N, Slobodianik N, Reinés A: Potentiation of omega-3 fatty acid antidepressant-like effects with low non-antidepressant doses of fluoxetine and mirtazapine. Eur J Pharmacol. 2010, 648 (1–3): 117-26.CrossRefPubMed Laino CH, Fonseca C, Sterin-Speziale N, Slobodianik N, Reinés A: Potentiation of omega-3 fatty acid antidepressant-like effects with low non-antidepressant doses of fluoxetine and mirtazapine. Eur J Pharmacol. 2010, 648 (1–3): 117-26.CrossRefPubMed
82.
go back to reference Sánchez-Villegas A, Delgado-Rodríguez M, Alonso A, Schlatter J, Lahortiga F, Serra Majem L, Martínez-González MA: Association of the Mediterranean dietary pattern with the incidence of depression: the Seguimiento Universidad de Navarra/University of Navarra follow-up (SUN) cohort. Arch Gen Psychiatry. 2009, 66 (10): 1090-8. 10.1001/archgenpsychiatry.2009.129.CrossRefPubMed Sánchez-Villegas A, Delgado-Rodríguez M, Alonso A, Schlatter J, Lahortiga F, Serra Majem L, Martínez-González MA: Association of the Mediterranean dietary pattern with the incidence of depression: the Seguimiento Universidad de Navarra/University of Navarra follow-up (SUN) cohort. Arch Gen Psychiatry. 2009, 66 (10): 1090-8. 10.1001/archgenpsychiatry.2009.129.CrossRefPubMed
83.
go back to reference Rienks J, Dobson AJ, Mishra GD: Mediterranean dietary pattern and prevalence and incidence of depressive symptoms in mid-aged women: results from a large community-based prospective study. Eur J Clin Nutr. 2013, 67 (1): 75-82. 10.1038/ejcn.2012.193.CrossRefPubMed Rienks J, Dobson AJ, Mishra GD: Mediterranean dietary pattern and prevalence and incidence of depressive symptoms in mid-aged women: results from a large community-based prospective study. Eur J Clin Nutr. 2013, 67 (1): 75-82. 10.1038/ejcn.2012.193.CrossRefPubMed
Metadata
Title
Long-term ω-3 fatty acid supplementation induces anti-stress effects and improves learning in rats
Authors
Miguel Á Pérez
Gonzalo Terreros
Alexies Dagnino-Subiabre
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Behavioral and Brain Functions / Issue 1/2013
Electronic ISSN: 1744-9081
DOI
https://doi.org/10.1186/1744-9081-9-25

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