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Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 22, 2019 - Issue 8
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Articles

Omega-3 fatty acid deficiency impairs frontostriatal recruitment following repeated amphetamine treatment in rats: A 7 Tesla in vivo phMRI study

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References

  • Crombag HS, Gorny G, Li Y, Kolb B, Robinson TE. Opposite effects of amphetamine self-administration experience on dendritic spines in the medial and orbital prefrontal cortex. Cereb Cortex 2005;15:341–8. doi: 10.1093/cercor/bhh136
  • Robinson TE, Kolb B. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur J Neurosci 1999;11:1598–604. doi: 10.1046/j.1460-9568.1999.00576.x
  • Robinson TE, Kolb B. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 1997;17:8491–7. doi: 10.1523/JNEUROSCI.17-21-08491.1997
  • Imperato A, Obinu MC, Carta G, Mascia MS, Casu MA, Gessa GL. Reduction of dopamine release and synthesis by repeated amphetamine treatment: role in behavioral sensitization. Eur J Pharmacol 1996;317:231–7. doi: 10.1016/S0014-2999(96)00742-X
  • Robinson TE, Jurson PA, Bennett JA, Bentgen KM. Persistent sensitization of dopamine neurotransmission in ventral striatum (nucleus accumbens) produced by prior experience with (+)-amphetamine: a microdialysis study in freely moving rats. Brain Res 1988;462:211–22. doi: 10.1016/0006-8993(88)90549-5
  • Scofield MD, Heinsbroek JA, Gipson CD, Kupchik YM, Spencer S, Smith AC, et al. The nucleus accumbens: mechanisms of addiction across drug classes reflect the importance of glutamate homeostasis. Pharmacol Rev 2016;68:816–71. doi: 10.1124/pr.116.012484
  • Lu W, Wolf ME. Repeated amphetamine administration alters AMPA receptor subunit expression in rat nucleus accumbens and medial prefrontal cortex. Synapse 1999;32:119–31. doi: 10.1002/(SICI)1098-2396(199905)32:2<119::AID-SYN5>3.0.CO;2-F
  • White FJ, Hu XT, Zhang XF, Wolf ME. Repeated administration of cocaine or amphetamine alters neuronal responses to glutamate in the mesoaccumbens dopamine system. J Pharmacol Exp Ther 1995;273:445–54.
  • Homayoun H, Moghaddam B. Progression of cellular adaptations in medial prefrontal and orbitofrontal cortex in response to repeated amphetamine. J Neurosci 2006;26:8025–39. doi: 10.1523/JNEUROSCI.0842-06.2006
  • Gulley JM, Stanis JJ. Adaptations in medial prefrontal cortex function associated with amphetamine-induced behavioral sensitization. Neuroscience 2010;166:615–24. doi: 10.1016/j.neuroscience.2009.12.044
  • Chang JC, Su KP, Mondelli V, Pariante CM. Omega-3 polyunsaturated fatty acids in youths with attention deficit hyperactivity disorder (ADHD): a systematic review and meta-analysis of clinical trials and biological studies. Neuropsychopharmacology 2017. [Epub ahead of print].
  • Bloch MH, Qawasmi A. Omega-3 fatty acid supplementation for the treatment of children with attention-deficit/hyperactivity disorder symptomatology: systematic review and meta-analysis. J Am Acad Child Adolesc Psychiatry 2011;50:991–1000. doi: 10.1016/j.jaac.2011.06.008
  • McNamara RK, Valentine CJ. Role of long-chain omega-3 fatty acids in cognitive and emotional development. In Dye L, Campoy C (eds.) Nutrition for brain health and cognitive performance. London: Taylor & Francis Group; 2015, p. 151–88.
  • Ahmad SO, Park JH, Radel JD, Levant B. Reduced numbers of dopamine neurons in the substantia nigra pars compacta and ventral tegmental area of rats fed an n-3 polyunsaturated fatty acid-deficient diet: a stereological study. Neurosci Lett 2008;438:303–7. doi: 10.1016/j.neulet.2008.04.073
  • Bondi CO, Taha AY, Tock JL, Totah NK, Cheon Y, Torres GE, et al. Adolescent behavior and dopamine availability are uniquely sensitive to dietary omega-3 fatty acid deficiency. Biol Psychiatry 2014;75:38–46. doi: 10.1016/j.biopsych.2013.06.007
  • Kodas E, Vancassel S, Lejeune B, Guilloteau D, Chalon S. Reversibility of n-3 fatty acid deficiency-induced changes in dopaminergic neurotransmission in rats: critical role of developmental stage. J Lipid Res 2002;43:1209–19.
  • Zimmer L, Vancassel S, Cantagrel S, Breton P, Delamanche S, Guilloteau D, et al. The dopamine mesocorticolimbic pathway is affected by deficiency in n-3 polyunsaturated fatty acids. Am J Clin Nutr 2002;75:662–7. doi: 10.1093/ajcn/75.4.662
  • Levant B, Radel JD, Carlson SE. Decreased brain docosahexaenoic acid during development alters dopamine-related behaviors in adult rats that are differentially affected by dietary remediation. Behav Brain Res 2004;152:49–57.
  • McNamara RK, Sullivan J, Richtand NM, Jandacek R, Rider T, Tso P, et al. Omega-3 fatty acid deficiency augments amphetamine-induced behavioral sensitization in adult DBA/2J mice: relationship with ventral striatum dopamine concentrations. Synapse 2008;62:725–35. doi: 10.1002/syn.20542
  • Cao D, Kevala K, Kim J, Moon HS, Jun SB, Lovinger D, et al. Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J Neurochem 2009;111:510–21. doi: 10.1111/j.1471-4159.2009.06335.x
  • McNamara RK, Asch RH, Schurdak JD, Lindquist DM. Glutamate homeostasis in the adult rat prefrontal cortex is altered by cortical docosahexaenoic acid accrual during adolescence: An in vivo 1H MRS study. Psychiatry Res 2017;270:39–45. doi: 10.1016/j.pscychresns.2017.10.003
  • Yoshida S, Yasuda A, Kawazato H, Sakai K, Shimada T, Takeshita M, et al. Synaptic vesicle ultrastructural changes in the rat hippocampus induced by a combination of alpha-linolenate deficiency and a learning task. J Neurochem 1997;68:1261–8. doi: 10.1046/j.1471-4159.1997.68031261.x
  • Grayson DS, Kroenke CD, Neuringer M, Fair DA. Dietary omega-3 fatty acids modulate large-scale systems organization in the rhesus macaque brain. J Neurosci 2014;34:2065–74. doi: 10.1523/JNEUROSCI.3038-13.2014
  • Sakamoto T, Cansev M, Wurtman RJ. Oral supplementation with docosahexaenoic acid and uridine-5′-monophosphate increases dendritic spine density in adult gerbil hippocampus. Brain Res 2007;1182:50–9. doi: 10.1016/j.brainres.2007.08.089
  • Chalon S, Delion-Vancassel S, Belzung C, Guilloteau D, Leguisquet AM, Besnard JC, et al. Dietary fish oil affects monoaminergic neurotransmission and behavior in rats. J Nutr 1998;128:2512–9. doi: 10.1093/jn/128.12.2512
  • Hess A, Stiller D, Kaulisch T, Heil P, Scheich H. New insights into the hemodynamic blood oxygenation level-dependent response through combination of functional magnetic resonance imaging and optical recording in gerbil barrel cortex. J Neurosci 2000;20:3328–38. doi: 10.1523/JNEUROSCI.20-09-03328.2000
  • Chen YC, Galpern WR, Brownell AL, Matthews RT, Bogdanov M, Isacson O, et al. Detection of dopaminergic neurotransmitter activity using pharmacologic MRI: correlation with PET, microdialysis, and behavioral data. Magn Reson Med 1997;38:389–98. doi: 10.1002/mrm.1910380306
  • Dixon AL, Prior M, Morris PM, Shah YB, Joseph MH, Young AM. Dopamine antagonist modulation of amphetamine response as detected using pharmacological MRI. Neuropharmacology 2005;48:236–45. doi: 10.1016/j.neuropharm.2004.10.006
  • Schwarz A, Gozzi A, Reese T, Bertani S, Crestan V, Hagan J, et al. Selective dopamine D(3) receptor antagonist SB-277011-A potentiates phMRI response to acute amphetamine challenge in the rat brain. Synapse 2004;54:1–10. doi: 10.1002/syn.20055
  • Schweinhardt P, Fransson P, Olson L, Spenger C, Andersson JL. A template for spatial normalisation of MR images of the rat brain. J Neurosci Methods 2003;129:105–13. doi: 10.1016/S0165-0270(03)00192-4
  • Jenkinson M, Smith SM. A global optimisation method for robust affine registration of brain images. Med Image Anal 2001;5:143–56. doi: 10.1016/S1361-8415(01)00036-6
  • Jenkinson M, Bannister P, Brady M, Smith S. Improved optimisation for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002;17:825–41. doi: 10.1006/nimg.2002.1132
  • Woolrich MW, Ripley BD, Brady JM, Smith SM. Temporal autocorrelation in univariate linear modelling of fMRI data. Neuroimage 2001;14:1370–86. doi: 10.1006/nimg.2001.0931
  • Worsley KJ. Statistical analysis of activation images. Ch 14. In Jezzard P, Matthews PM, Smith SM (eds.) Functional MRI: an introduction to methods. Oxford : Oxford University Press; 2001.
  • McNamara RK, Able J, Jandacek R, Rider T, Tso P. Inbred C57BL/6J and DBA/2J mouse strains exhibit constitutive differences in regional brain fatty acid composition. Lipids 2009;44:1–8. doi: 10.1007/s11745-008-3244-8
  • Schrantee A, Tremoleda JL, Wylezinska-Arridge M, Bouet V, Hesseling P, Meerhoff GF, et al. Repeated dexamphetamine treatment alters the dopaminergic system and increases the phMRI response to methylphenidate. PLoS One 2017;12:e0172776. doi: 10.1371/journal.pone.0172776
  • van der Marel K, Klomp A, Meerhoff GF, Schipper P, Lucassen PJ, Homberg JR, et al. Long-term oral methylphenidate treatment in adolescent and adult rats: differential effects on brain morphology and function. Neuropsychopharmacology 2014;39:263–73. doi: 10.1038/npp.2013.169
  • Advokat C. Update on amphetamine neurotoxicity and its relevance to the treatment of ADHD. J Atten Disord 2007;11:8–16. doi: 10.1177/1087054706295605
  • Bousquet M, Gue K, Emond V, Julien P, Kang JX, Cicchetti F, et al. Transgenic conversion of omega-6 into omega-3 fatty acids in a mouse model of Parkinson’s disease. J Lipid Res 2011;52:263–71. doi: 10.1194/jlr.M011692
  • Ozsoy O, Seval-Celik Y, Hacioglu G, Yargicoglu P, Demir R, Agar A, Aslan M. The influence and the mechanism of docosahexaenoic acid on a mouse model of Parkinson’s disease. Neurochem Int 2011;59:664–70. doi: 10.1016/j.neuint.2011.06.012
  • Tanriover G, Seval-Celik Y, Ozsoy O, Akkoyunlu G, Savcioglu F, Hacioglu G, et al. The effects of docosahexaenoic acid on glial derived neurotrophic factor and neurturin in bilateral rat model of Parkinson’s disease. Folia Histochem Cytobiol 2010;48:434–41. doi: 10.2478/v10042-010-0047-6
  • McNamara RK, Rider T, Jandacek RJ, Tso P, Cole-Strauss A, Lipton JW. Omega-3 fatty acid deficiency increases constitutive pro-inflammatory cytokine production in rats: relationship with central serotonin turnover. Prostaglandins Leukot Essent Fatty Acids 2010;83:185–91. doi: 10.1016/j.plefa.2010.08.004
  • Cubillo A, Halari R, Giampietro V, Taylor E, Rubia K. Fronto-striatal underactivation during interference inhibition and attention allocation in grown up children with attention deficit/hyperactivity disorder and persistent symptoms. Psychiatry Res 2011;193:17–27. doi: 10.1016/j.pscychresns.2010.12.014
  • Hart H, Radua J, Nakao T, Mataix-Cols D, Rubia K. Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry 2013;70:185–98. doi: 10.1001/jamapsychiatry.2013.277
  • Rubia K, Halari R, Cubillo A, Mohammad AM, Brammer M, Taylor E. Methylphenidate normalises activation and functional connectivity deficits in attention and motivation networks in medication-naïve children with ADHD during a rewarded continuous performance task. Neuropharmacology 2009;57:640–52. doi: 10.1016/j.neuropharm.2009.08.013
  • Rubia K, Halari R, Mohammad AM, Taylor E, Brammer M. Methylphenidate normalizes frontocingulate underactivation during error processing in attention-deficit/hyperactivity disorder. Biol Psychiatry 2011;70:255–62. doi: 10.1016/j.biopsych.2011.04.018
  • Vaidya CJ, Austin G, Kirkorian G, Ridlehuber HW, Desmond JE, Glover GH, et al. Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. Proc Natl Acad Sci USA 1998;95:14494–9. doi: 10.1073/pnas.95.24.14494
  • Thompson TL, Moss RL. In vivo stimulated dopamine release in the nucleus accumbens: modulation by the prefrontal cortex. Brain Res 1995;686:93–8. doi: 10.1016/0006-8993(95)00429-T
  • Jaskiw GE, Karoum F, Freed WJ, Phillips I, Kleinman JE, Weinberger DR. Effect of ibotenic acid lesions of the medial prefrontal cortex on amphetamine-induced locomotion and regional brain catecholamine concentrations in the rat. Brain Res 1990;534:263–72. doi: 10.1016/0006-8993(90)90138-2

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