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Research Article| Volume 88, ISSUE 6, P419-429, June 2013

Omega-3 fatty acids are related to abnormal emotion processing in adolescent boys with attention deficit hyperactivity disorder

      Abstract

      Background

      In addition to the core symptoms, attention deficit hyperactivity disorder (ADHD) is associated with poor emotion regulation. There is some evidence that children and young adults with ADHD have lower omega-3 levels and that supplementation with omega-3 can improve both ADHD and affective symptoms. We therefore investigated differences between ADHD and non-ADHD children in omega-3/6 fatty acid plasma levels and the relationship between those indices and emotion-elicited event-related potentials (ERPs).

      Methods

      Children/adolescents with (n=31) and without ADHD (n=32) were compared in their plasma omega-3/6 indices and corresponding ERPs during an emotion processing task.

      Results

      Children with ADHD had lower mean omega-3/6 and ERP abnormalities in emotion processing, independent of emotional valence relative to control children. ERP abnormalities were significantly associated with lower omega-3 levels in the ADHD group.

      Conclusions

      The findings reveal for the first time that lower omega-3 fatty acids are associated with impaired emotion processing in ADHD children.

      Abbreviations:

      ERPs (event-related potentials), LC-PUFA (long-chain polyunsaturated fatty acids), EPA (eicosapentaenoic acid), DHA (docosahexaenoic acid), AA (arachidonic acid), ADHD (attention deficit hyperactivity disorder)

      Keywords

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      References

        • Taylor E.
        • Dopfner M.
        • Sergeant J.
        • Asherson P.
        • Banaschewski T.
        • Buitelaar J.
        • Coghill D.
        • Danckaerts M.
        • Rothenberger A.
        • Sonuga-Barke E.
        • Steinhausen H.C.
        • Zuddas A.
        European clinical guidelines for hyperkinetic disorder—first upgrade.
        Eur. Child Adolesc. Psychiatry. 2004; 13: I7-30
        • Rubia K.
        Cool inferior frontostriatal dysfunction in attention-deficit/hyperactivity disorder versus hot ventromedial orbitofrontal–limbic dysfunction in conduct disorder: a review.
        Biol. Psychiatry. 2011; 69: e69-87
        • 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.
        Arch. Gen. Psychiatry. 2012; : 1-14
        • Schlochtermeier L.
        • Stoy M.
        • Schlagenhauf F.
        • Wrase J.
        • Park S.Q.
        • Friedel E.
        • Huss M.
        • Lehmkuhl U.
        • Heinz A.
        • Strohle A.
        Childhood methylphenidate treatment of ADHD and response to affective stimuli.
        Eur. Neuropsychopharmacol. 2011; 21: 646-654
        • Greene R.W.
        • Biederman J.
        • Faraone S.V.
        • Monuteaux M.C.
        • Mick E.
        • DuPre E.P.
        • Fine C.S.
        • Goring J.C.
        Social impairment in girls with ADHD: patterns, gender comparisons, and correlates.
        J. Am. Acad. Child Adolesc. Psychiatry. 2001; 40: 704-710
        • de Boo G.M.
        • Prins P.J.M.
        Social incompetence in children with ADHD: Possible moderators and mediators in social-skills training.
        Clinical Psychology Review. 2007; 27: 78-97
        • Singh S.D.
        • Ellis C.R.
        • Winton A.S.
        • Singh N.N.
        • Leung J.P.
        • Oswald D.P.
        Recognition of facial expressions of emotion by children with attention-deficit hyperactivity disorder.
        Behav. Modif. 1998; 22: 128-142
        • Pelc K.
        • Kornreich C.
        • Foisy M.L.
        • Dan B.
        Recognition of emotional facial expressions in attention-deficit hyperactivity disorder.
        Pediatr. Neurol. 2006; 35: 93-97
        • Sinclair A.J.
        • Crawford M.A.
        The accumulation of arachidonate and docosahexaenoate in the developing rat brain.
        J. Neurochem. 1972; 19: 1753-1758
        • Sinclair A.J.
        • Crawford M.A.
        The incorporation of linolenic aid and docosahexaenoic acid into liver and brain lipids of developing rats.
        FEBS Lett. 1972; 26: 127-129
        • Fiennes R.N.
        • Sinclair A.J.
        • Crawford M.A.
        Essential fatty acid studies in primates linolenic acid requirements of capuchins.
        J. Med. Primatol. 1973; 2: 155-169
        • Freeman M.P.
        • Hibbeln J.R.
        • Wisner K.L.
        • Davis J.M.
        • Mischoulon D.
        • Peet M.
        • Keck Jr., P.E.
        • Marangell L.B.
        • Richardson A.J.
        • Lake J.
        • Stoll A.L.
        Omega-3 fatty acids: evidence basis for treatment and future research in psychiatry.
        J. Clin. Psychiatry. 2006; 67: 1954-1967
        • Zimmer L.
        • Delpal S.
        • Guilloteau D.
        • Aioun J.
        • Durand G.
        • Chalon S.
        Chronic n-3 polyunsaturated fatty acid deficiency alters dopamine vesicle density in the rat frontal cortex.
        Neurosci. Lett. 2000; 284: 25-28
        • Chalon S.
        Omega-3 fatty acids and monoamine neurotransmission.
        Prostaglandins, Leukot. Essent. Fatty Acids. 2006; 75: 259-269
        • Conklin S.M.
        • Manuck S.B.
        • Yao J.K.
        • Flory J.D.
        • Hibbeln J.R.
        • Muldoon M.F.
        High omega-6 and low omega-3 fatty acids are associated with depressive symptoms and neuroticism.
        Psychosom. Med. 2007; 69: 932-934
        • Antalis C.J.
        • Stevens L.J.
        • Campbell M.
        • Pazdro R.
        • Ericson K.
        • Burgess J.R.
        Omega-3 fatty acid status in attention-deficit/hyperactivity disorder.
        Prostaglandins Leukot. Essen. Fatty Acids. 2006; 75: 299-308
        • Stevens L.J.
        • Zentall S.S.
        • Deck J.L.
        • Abate M.L.
        • Watkins B.A.
        • Lipp S.R.
        • Burgess J.R.
        Essential fatty acid metabolism in boys with attention-deficit hyperactivity disorder.
        Am. J Clin. Nutr. 1995; 62: 761-768
        • Young G.S.
        • Maharaj N.J.
        • Conquer J.A.
        Blood phospholipid fatty acid analysis of adults with and without attention deficit/hyperactivity disorder.
        Lipids. 2004; 39: 117-123
        • Spahis S.
        • Vanasse M.
        • Bélanger S.A.
        • Ghadirian P.
        • Grenier E.
        • Levy E.
        Lipid profile, fatty acid composition and pro- and anti-oxidant status in pediatric patients with attention-deficit/hyperactivity disorder.
        Prostaglandins Leukot. Essent. Fatty Acids. 2008; 79: 47-53
        • Mitchell E.A.
        • Lewis S.
        • Cutler D.R.
        Essential fatty acids and maladjusted behaviour in children.
        Prostaglandins Leukot. Med. 1983; 12: 281-287
        • Bloch M.H.
        • 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
        • Nemets H.
        • Nemets B.
        • Apter A.
        • Bracha Z.
        • Belmaker R.H.
        Omega-3 treatment of childhood depression: a controlled, double-blind pilot study.
        Am. J. Psychiatry. 2006; 163: 1098-1100
        • Zaalberg A.
        • Nijman H.
        • Bulten E.
        • Stroosma L.
        • van der Staak C.
        Effects of nutritional supplements on aggression, rule-breaking, and psychopathology among young adult prisoners.
        Aggressive Behavior. 2010; 36: 117-126
        • Gesch C.B.
        • Hammond S.M.
        • Hampson S.E.
        • Eves A.
        • Crowder M.J.
        Influence of supplementary vitamins, minerals and essential fatty acids on the antisocial behaviour of young adult prisoners. Randomised, placebo-controlled trial.
        Br. J. Psychiatry. 2002; 181: 22-28
        • Jazayeri S.
        • Tehrani-Doost M.
        • Keshavarz S.A.
        • Hosseini M.
        • Djazayery A.
        • Amini H.
        • Jalali M.
        • Peet M.
        Comparison of therapeutic effects of omega-3 fatty acid eicosapentaenoic acid and fluoxetine, separately and in combination, in major depressive disorder.
        Aust. N. Z. J. Psychiatry. 2008; 42: 192-198
        • Peet M.
        • Horrobin D.F.
        A dose-ranging study of the effects of ethyl-eicosapentaenoate in patients with ongoing depression despite apparently adequate treatment with standard drugs.
        Arch. Gen. Psychiatry. 2002; 59: 913-919
        • Gow R.V.
        • Matsudaira T.
        • Taylor E.
        • Rubia K.
        • Crawford M.
        • Ghebremeskel K.
        • Ibrahimovic A.
        • Vallee-Tourangeau F.
        • Williams L.M.
        • Sumich A.
        Total red blood cell concentrations of omega-3 fatty acids are associated with emotion-elicited neural activity in adolescent boys with attention-deficit hyperactivity disorder.
        Prostaglandins Leukot. Essent. Fatty Acids. 2009; 80: 151-156
        • Luck S.
        An Introduction to the Event-Related Potential Technique (Cognitive Neuroscience).
        The MIT Press, 2005
        • Rellecke J.
        • Sommer W.
        • Schacht A.
        Does processing of emotional facial expressions depend on intention? Time-resolved evidence from event-related brain potentials.
        Biol. Psychol. 2012;
        • Brotman M.A.
        • Rich B.A.
        • Guyer A.E.
        • Lunsford J.R.
        • Horsey S.E.
        • Reising M.M.
        • Thomas L.A.
        • Fromm S.J.
        • Towbin K.
        • Pine D.S.
        • Leibenluft E.
        Amygdala activation during emotion processing of neutral faces in children with severe mood dysregulation versus ADHD or bipolar disorder.
        Am. J. Psychiatry. 2010; 167: 61-69
        • Dickstein D.P.
        • Castellanos F.X.
        Face Processing in Attention Deficit/Hyperactivity Disorder. 2012; (in): 1-19
        • Marsh A.A.
        • Finger E.C.
        • Michell D.G.V.
        • Sims C.
        • Kosson D.S.
        • Towbin K.E.
        • Leibenluft E.
        • Pine D.S.
        • Blair R.J.S.
        Reduced amygdala resonse to fearful expressions in children and adolescents with callous-unemotional traits and disruptive behaviour disorders.
        Am. J. Psychiatry. 2008; 165: 712-720
        • Williams L.M.
        • Hermens D.F.
        • Palmer D.
        • Kohn M.
        • Clarke S.
        • Keage H.
        • Clark C.R.
        • Gordon E.
        Misinterpreting emotional expressions in attention-deficit/hyperactivity disorder: evidence for a neural marker and stimulant effects.
        Biol. Psychiatry. 2008; 63: 917-926
        • Singhal A.
        • Shafer A.T.
        • Russell M.
        • Gibson B.
        • Wang L.
        • Vohra S.
        • Dolcos F.
        Electrophysiological correlates of fearful and sad distraction on target processing in adolescents with attention deficit-hyperactivity symptoms and affective disorders.
        Front Integr. Neurosci. 2012; 6: 119
        • Halgren E.
        • Baudena P.
        • Heit G.
        • Clarke J.M.
        • Marinkovic K.
        • Chauvel P.
        • Clarke M.
        Spatio-temporal stages in face and word processing. 2. Depth-recorded potentials in the human frontal and Rolandic cortices.
        J. Physiol. Paris. 1994; 88: 51-80
        • Liddell B.J.
        • Williams L.M.
        • Rathjen J.
        • Shevrin H.
        • Gordon E.
        A temporal dissociation of subliminal versus supraliminal fear perception: an event-related potential study.
        J. Cogn. Neurosci. 2004; 16: 479-486
        • Kiefer M.
        • Spitzer M.
        Time course of conscious and unconscious semantic brain activation.
        Neuroreport. 2000; 11: 2401-2407
        • Jonkman L.M.
        The development of preparation, conflict monitoring and inhibition from early childhood to young adulthood: a Go/Nogo ERP study.
        Brain Res. 2006; 1097: 181-193
        • Pliszka S.R.
        • Liotti M.
        • Woldorff M.G.
        Inhibitory control in children with attention-deficit/hyperactivity disorder: event-related potentials identify the processing component and timing of an impaired right-frontal response-inhibition mechanism.
        Biol. Psychiatry. 2000; 48: 238-246
        • Liotti M.
        • Pliszka S.R.
        • Perez 3rd, R.
        • Luus B.
        • Glahn D.
        • Semrud-Clikeman M.
        Electrophysiological correlates of response inhibition in children and adolescents with ADHD: influence of gender, age, and previous treatment history.
        Psychophysiology. 2007; 44: 936-948
        • Jonkman L.M.
        • Kemner C.
        • Verbaten M.N.
        • Koelega H.S.
        • Camfferman G.
        • vd Gaag R.J.
        • Buitelaar J.K.
        • van Engeland H.
        Event-related potentials and performance of attention-deficit hyperactivity disorder: children and normal controls in auditory and visual selective attention tasks.
        Biol. Psychiatry. 1997; 41: 595-611
        • Dimoska A.
        • Johnstone S.J.
        • Barry R.J.
        • Clarke A.R.
        Inhibitory motor control in children with attention-deficit/hyperactivity disorder: event-related potentials in the stop-signal paradigm.
        Biol. Psychiatry. 2003; 54: 1345-1354
      1. I.H. Shen, S.-Y. Tsai, J.-R. Duann, Inhibition control and error processing in children with attention deficit/hyperactivity disorder: an event-related potentials study, Int. J. Psychophysiol. 81 (2011) 1–11, 10.1016/j.ijpsycho.2011.03.015

        • Brandeis D.
        • van Leeuwen T.H.
        • Rubia K.
        • Vitacco D.
        • Steger J.
        • Pascual-Marqui R.D.
        • Steinhausen H.C.
        Neuroelectric mapping reveals precursor of stop failures in children with attention deficits.
        Behav. Brain Res. 1998; 94: 111-125
        • Banaschewski T.
        • Brandeis D.
        • Heinrich H.
        • Albrecht B.
        • Brunner E.
        • Rothenberger A.
        Questioning inhibitory control as the specific deficit of ADHD—evidence from brain electrical activity.
        J. Neural Transm. 2004; 111: 841-864
        • Fallgatter A.J.
        • Ehlis A.C.
        • Seifert J.
        • Strik W.K.
        • Scheuerpflug P.
        • Zillessen K.E.
        • Herrmann M.J.
        • Warnke A.
        Altered response control and anterior cingulate function in attention-deficit/hyperactivity disorder boys.
        Clin. Neurophysiol. 2004; 115: 973-981
      2. D. Brandeis, T.H. van Leeuwen, J. Steger, K. Imhof, H.-C. Steinhausen, Mapping brain functions of ADHD children, in: International Congress Series, vol. 1232, 2002, pp. 649–654.

      3. M.T. Rooney, E.B. Weller, Administration Manual for the Chips: Children's Interview for Psychiatric Syndromes, American Psychiatric Pub Incorporated, 1999.

        • Folch J.
        • Lees M.
        • Stanley G.H.Sloane
        A simple method for the isolation and purification of total lipides from animal tissues.
        J. Biol. Chem. 1957; 226: 497-509
        • Bueno A.A.
        • Ghebremeskel K.
        • Bakheit K.H.
        • Elbashir M.I.
        • Adam I.
        Dimethyl acetals, an indirect marker of the endogenous antioxidant plasmalogen level, are reduced in blood lipids of Sudanese pre-eclamptic subjects whose background diet is high in carbohydrate.
        J. Obstet. Gynaecol. 2012; 32: 241-246
        • Gur R.C.
        • Sara R.
        • Hagendoorn M.
        • Marom O.
        • Hughett P.
        • Macy L.
        • Turner T.
        • Bajcsy R.
        • Posner A.
        • Gur R.E.
        A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies.
        J. Neurosci. Methods. 2002; 115: 137-143
        • Gratton G.
        • Coles M.G.
        • Donchin E.
        A new method for off-line removal of ocular artifact.
        Electroencephalogr. Clin. Neurophysiol. 1983; 55: 468-484
        • Benjamini Y.
        • Hochberg Y.
        Controlling the false discovery rate—a practical and powerful approach to multiple testing.
        J. R. Stat. Soc. Ser. B—Methodol. 1995; 57: 289-300
        • Kuntsi J.
        • Eley T.C.
        • Taylor A.
        • Hughes C.
        • Asherson P.
        • Caspi A.
        • Moffitt T.E.
        Co-occurrence of ADHD and low IQ has genetic origins.
        Am. J. Med. Genet. Part B: Neuropsychiatric Genet. 2004; 124B: 41-47
        • Miller G.A.
        • Chapman J.P.
        Misunderstanding analysis of covariance.
        J. Abnorm. Psychol. 2001; 110: 40-48
        • Dennis M.
        • Francis D.J.
        • Cirino P.T.
        • Schachar R.
        • Barnes M.A.
        • Fletcher J.M.
        • Why IQ
        is not a covariate in cognitive studies of neurodevelopmental disorders.
        J. Int. Neuropsychol. Soc. 2009; 15: 331-343
        • Hofacer R.
        • Jandacek R.
        • Rider T.
        • Tso P.
        • Magrisso I.J.
        • Benoit S.C.
        • McNamara R.K.
        Omega-3 fatty acid deficiency selectively up-regulates delta6-desaturase expression and activity indices in rat liver: prevention by normalization of omega-3 fatty acid status.
        Nutr. Res. 2011; 31: 715-722
        • Nakamura M.T.
        • Nara T.Y.
        Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases.
        Annu. Rev. Nutr. 2004; 24: 345-376
        • Steer C.D.
        • Hibbeln J.R.
        • Golding J.
        • Davey Smith G.
        Polyunsaturated fatty acid levels in blood during pregnancy, at birth and at 7 years: their associations with two common FADS2 polymorphisms.
        Human Mol. Genet. 2012;
        • Brookes K.J.
        • Chen W.
        • Xu X.
        • Taylor E.
        • Asherson P.
        Association of fatty acid desaturase genes with attention-deficit/hyperactivity disorder.
        Biol. Psychiatry. 2006; 60: 1053-1061
        • Bentin S.
        • Allison T.
        • Puce A.
        • Perez E.
        • McCarthy G.
        Electrophysiological studies of face perception in humans.
        J. Cogn. Neurosci. 1996; 8: 551-565
        • Ibanez A.
        • Petroni A.
        • Urquina H.
        • Torrente F.
        • Torralva T.
        • Hurtado E.
        • Guex R.
        • Blenkmann A.
        • Beltrachini L.
        • Muravchik C.
        • Baez S.
        • Cetkovich M.
        • Sigman M.
        • Lischinsky A.
        • Manes F.
        Cortical deficits of emotional face processing in adults with ADHD: its relation to social cognition and executive function.
        Soc. Neurosci. 2011; 6: 464-481
        • Pollak S.D.
        • Klorman R.
        • Thatcher J.E.
        • Cicchetti D.
        P3b reflects maltreated children's reactions to facial displays of emotion.
        Psychophysiology. 2001; 38: 267-274
        • Meier N.M.
        • Perrig W.
        • Koenig T.
        Neurophysiological correlates of delinquent behaviour in adult subjects with ADHD.
        Int. J. Psychophysiol. 2012; 84: 1-16
        • Barry R.J.
        • Clarke A.R.
        • McCarthy R.
        • Selikowitz M.
        • Brown C.R.
        • Heaven P.C.L.
        Event-related potentials in adults with attention-deficit/hyperactivity disorder: an investigation using an inter-modal auditory/visual oddball task.
        Int. J. Psychophysiol. 2009; 71: 124-131
        • Schutter D.J.
        • de Haan E.H.
        • van Honk J.
        Functionally dissociated aspects in anterior and posterior electrocortical processing of facial threat.
        Int. J. Psychophysiol. 2004; 53: 29-36
        • Eimer M.
        • Holmes A.
        An ERP study on the time course of emotional face processing.
        Neuroreport. 2002; 13: 427-431
        • Ashley V.
        • Vuilleumier P.
        • Swick D.
        Time course and specificity of event-related potentials to emotional expressions.
        Neuroreport. 2004; 15: 211-216
        • Pizzagalli D.A.
        • Lehmann D.
        • Hendrick A.M.
        • Regard M.
        • Pascual-Marqui R.D.
        • Davidson R.J.
        Affective judgments of faces modulate early activity (approximately 160 ms) within the fusiform gyri.
        Neuroimage. 2002; 16: 663-677
        • Banaschewski T.
        • Ruppert S.
        • Tannock R.
        • Albrecht B.
        • Becker A.
        • Uebel H.
        • Sergeant J.A.
        • Rothenberger A.
        Colour perception in ADHD.
        J. Child Psychol. Psychiatry. 2006; 47: 568-572
        • Banaschewski T.
        • Brandeis D.
        • Heinrich H.
        • Albrecht B.
        • Brunner E.
        • Rothenberger A.
        Association of ADHD and conduct disorder—brain electrical evidence for the existence of a distinct subtype.
        J. Child Psychol. Psychiatry Allied Disciplines. 2003; 44: 356-376
        • van Leeuwen T.H.
        • Steinhausen H.C.
        • Overtoom C.C.
        • Pascual-Marqui R.D.
        • van't Klooster B.
        • Rothenberger A.
        • Sergeant J.A.
        • Brandeis D.
        The continuous performance test revisited with neuroelectric mapping: impaired orienting in children with attention deficits.
        Behav. Brain Res. 1998; 94: 97-110
        • Condray R.
        • Yao J.K.
        • Steinhauer S.R.
        • van Kammen D.P.
        • Reddy R.D.
        • Morrow L.A.
        Semantic memory in schizophrenia: association with cell membrane essential fatty acids.
        Schizophr. Res. 2008; 106: 13-28
        • Boucher O.
        • Burden M.J.
        • Muckle G.
        • Saint-Amour D.
        • Ayotte P.
        • Dewailly E.
        • Nelson C.A.
        • Jacobson S.W.
        • Jacobson J.L.
        Neurophysiologic and neurobehavioral evidence of beneficial effects of prenatal omega-3 fatty acid intake on memory function at school age.
        Am. J. Clin. Nutr. 2011; 93: 1025-1037
        • Yehuda S.
        • Rabinovitz S.
        • Mostofsky D.I.
        Essential fatty acids are mediators of brain biochemistry and cognitive functions.
        J. Neurosci. Res. 1999; 56: 565-570
        • Yavin E.
        • Himovichi E.
        • Eilam R.
        Delayed cell migration in the developing rat brain following maternal omega 3 alpha linolenic acid dietary deficiency.
        Neuroscience. 2009; 162: 1011-1022
        • Tripp G.
        • Wickens J.R.
        Research review: dopamine transfer deficit: a neurobiological theory of altered reinforcement mechanisms in ADHD.
        J. Child Psychol. Psychiatry. 2008; 49: 691-704
        • Blasbalg T.L.
        • Hibbeln J.R.
        • Ramsden C.E.
        • Majchrzak S.F.
        • Rawlings R.R.
        Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century.
        Am. J. Clin. Nutr. 2011; 93: 950-962
        • Hibbeln J.R.
        From homicide to happiness—a commentary on omega-3 fatty acids in human society.
        Cleave Award Lecture, Nutr Health. 2007; 19: 9-19
        • Hibbeln J.R.
        Seafood consumption and homicide mortality. A cross-national ecological analysis.
        World Rev. Nutr. Diet. 2001; 88: 41-46