Mitochondrial function in the brain links anxiety with social subordination

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 50, 2015, Pages 15486-15491

  Hollis, Fiona ^a   Van Der Kooij, Michael A ^a,c   Zanoletti, Olivia ^a   Lozano, Laura ^a   Cantó, Carles ^b   Sandi, Carmen ^a  

^a EPFL   (Switzerland)

^b NESTLÉ RESEARCH CENTER   (Switzerland)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Anxiety; Mitochondria; Nucleus accumbens; Social competition; Social dominance

Indexed keywords

ADENOSINE TRIPHOSPHATE; NICOTINAMIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); MULTIENZYME COMPLEX;

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BRAIN METABOLISM; BRAIN MITOCHONDRION; CONTROLLED STUDY; ENZYME INHIBITION; INTRA-ACCUMBAL DRUG ADMINISTRATION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; OUTBRED RAT STRAIN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SOCIAL DOMINANCE; SOCIAL INTERACTION; SOCIAL STATUS; ANIMAL; BRAIN; DOMINANT-SUBORDINATE RELATIONSHIP; METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; SOCIAL BEHAVIOR; WISTAR RAT;

ANIMALS; ANXIETY; BRAIN; DOMINANCE-SUBORDINATION; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; MALE; MITOCHONDRIA; NIACINAMIDE; NUCLEUS ACCUMBENS; RATS, WISTAR; SOCIAL BEHAVIOR;

EID: 84950326915     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1512653112     Document Type: Article

References (60)

1. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308(5722):648-652.
2. Neumann ID, Veenema AH, Beiderbeck DI (2010) Aggression and anxiety: Social context and neurobiological links. Front Behav Neurosci 4:12.
3. Fuxjager MJ, et al. (2010) Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc Natl Acad Sci USA 107(27):12393-12398.
4. Oliveira RF, Silva A, Canario AV (2009) Why do winners keep winning? Androgen mediation of winner but not loser effects in cichlid fish. Proc Biol Sci 276(1665):2249-2256.
5. Boyce WT (2004) Social stratification, health, and violence in the very young. Ann N Y Acad Sci 1036:47-68.
6. Allan S, Gilbert P (1997) Submissive behaviour and psychopathology. Br J Clin Psychol 36(Pt 4):467-488.
7. Gilbert P, McEwan K, Bellew R, Mills A, Gale C (2009) The dark side of competition: How competitive behaviour and striving to avoid inferiority are linked to depression, anxiety, stress and self-harm. Psychol Psychother 82(Pt 2):123-136.
8. Goette L, Bendahan S, Thoresen J, Hollis F, Sandi C (2015) Stress pulls us apart: Anxiety leads to differences in competitive confidence under stress. Psychoneuroendocrinology 54:115-123.
9. Tyrka AR, et al. (2015) Alterations of mitochondrial DNA copy number and telomere length with early adversity and psychopathology. Biol Psychiatry, 10.1016/j.biopsych.2014.12.025.
10. Streck EL, et al. (2014) Mitochondria and the central nervous system: Searching for a pathophysiological basis of psychiatric disorders. Rev Bras Psiquiatr 36(2):156-167.
11. Morava E, Kozicz T (2013) Mitochondria and the economy of stress (mal) adaptation. Neurosci Biobehav Rev 37(4):668-680.
12. Anglin RE, Mazurek MF, Tarnopolsky MA, Rosebush PI (2012) The mitochondrial genome and psychiatric illness. Am J Med Genet B Neuropsychiatr Genet 159 B (7): 749-759.
13. Morava E, et al. (2010) Depressive behaviour in children diagnosed with a mitochondrial disorder. Mitochondrion 10(5):528-533.
14. Koene S, et al. (2009) Major depression in adolescent children consecutively diagnosed with mitochondrial disorder. J Affect Disord 114(1-3):327-332.
15. Wang F, et al. (2011) Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science 334(6056):693-697.
16. Beiderbeck DI, et al. (2012) High and abnormal forms of aggression in rats with extremes in trait anxiety-involvement of the dopamine system in the nucleus accumbens. Psychoneuroendocrinology 37(12):1969-1980.
17. Kumaran D, Melo HL, Duzel E (2012) The emergence and representation of knowledge about social and nonsocial hierarchies. Neuron 76(3):653-666.
18. Machado CJ, Bachevalier J (2006) The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). Behav Neurosci 120(4):761-786.
19. Zink CF, et al. (2008) Know your place: Neural processing of social hierarchy in humans. Neuron 58(2):273-283.
20. Ly M, Haynes MR, Barter JW, Weinberger DR, Zink CF (2011) Subjective socioeconomic status predicts human ventral striatal responses to social status information. Curr Biol 21(9):794-797.
21. Le Bouc R, Pessiglione M (2013) Imaging social motivation: Distinct brain mechanisms drive effort production during collaboration versus competition. J Neurosci 33(40):15894-15902.
22. Wilensky AE, Schafe GE, LeDoux JE (1999) Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. J Neurosci 19(24):RC48.
23. Le Moine C, Bloch B (1995) D1 and D2 dopamine receptor gene expression in the rat striatum: Sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J Comp Neurol 355(3):418-426.
24. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80(1):315-360.
25. Cheng A, Hou Y, Mattson MP (2010) Mitochondria and neuroplasticity. ASN Neuro 2(5):e00045.
26. Manji H, et al. (2012) Impaired mitochondrial function in psychiatric disorders. Nat Rev Neurosci 13(5):293-307.
27. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11(1):81-128.
28. Houtkooper RH, Cantó C, Wanders RJ, Auwerx J (2010) The secret life of NAD+: An old metabolite controlling new metabolic signaling pathways. Endocr Rev 31(2):194-223.
29. Nowak R, et al. (2010) Effect of selected NAD+ analogues on mitochondria activity and proliferation of endothelial EA. hy926 cells. Eur J Pharmacol 640(1-3):102-111.
30. Murphy MP, Smith RA (2007) Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu Rev Pharmacol Toxicol 47:629-656.
31. Gardner A, Boles RG (2011) Beyond the serotonin hypothesis: Mitochondria, inflammation and neurodegeneration in major depression and affective spectrum disorders. Prog Neuropsychopharmacol Biol Psychiatry 35(3):730-743.
32. Picard M, Juster RP, McEwen BS (2014) Mitochondrial allostatic load puts the 'gluc' back in glucocorticoids. Nat Rev Endocrinol 10(5):303-310.
33. Fantin G, Bottecchia D (1984) Effect of nucleus accumbens destruction in rat. Experientia 40(6):573-575.
34. Anstrom KK, Miczek KA, Budygin EA (2009) Increased phasic dopamine signaling in the mesolimbic pathway during social defeat in rats. Neuroscience 161(1):3-12.
35. Pucitowski O, Trzaskowska E, Kostowski W, Wosko W (1988) Inhibition of affective aggression and dominance in rats after thyrotropin-releasing hormone (TRH) microinjection into the nucleus accumbens. Peptides 9(3):539-543.
36. Bhanji JP, Delgado MR (2014) The social brain and reward: Social information processing in the human striatum. Wiley Interdiscip Rev Cogn Sci 5(1):61-73.
37. Robbins TW, Everitt BJ (2007) A role for mesencephalic dopamine in activation: Commentary on Berridge (2006). Psychopharmacology (Berl) 191(3):433-437.
38. Beeler JA, Frazier CR, Zhuang X (2012) Putting desire on a budget: Dopamine and energy expenditure, reconciling reward and resources. Front Integr Nuerosci 6:49.
39. Niv Y, Daw ND, Joel D, Dayan P (2007) Tonic dopamine: Opportunity costs and the control of response vigor. Psychopharmacology (Berl) 191(3):507-520.
40. Salamone JD, Correa M, Nunes EJ, Randall PA, Pardo M (2012) The behavioral pharmacology of effort-related choice behavior: Dopamine, adenosine and beyond. J Exp Anal Behav 97(1):125-146.
41. Treadway MT, Bossaller NA, Shelton RC, Zald DH (2012) Effort-based decision-making in major depressive disorder: A translational model of motivational anhedonia. J Abnorm Psychol 121(3):553-558.
42. Floresco SB (2015) The nucleus accumbens: An interface between cognition, emotion, and action. Annu Rev Psychol 66:25-52.
43. Bodnar LM, Wisner KL (2005) Nutrition and depression: Implications for improving mental health among childbearing-aged women. Biol Psychiatry 58(9):679-685.
44. Liu D, et al. (2013) Nicotinamide forestalls pathology and cognitive decline in Alzheimer mice: Evidence for improved neuronal bioenergetics and autophagy procession. Neurobiol Aging 34(6):1564-1580.
45. Einat H, Yuan P, Manji HK (2005) Increased anxiety-like behaviors and mitochondrial dysfunction in mice with targeted mutation of the Bcl-2 gene: Further support for the involvement of mitochondrial function in anxiety disorders. Behav Brain Res 165(2):172-180.
46. Hovatta I, et al. (2005) Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438(7068):662-666.
47. Rammal H, Bouayed J, Younos C, Soulimani R (2008) Evidence that oxidative stress is linked to anxiety-related behaviour in mice. Brain Behav Immun 22(8):1156-1159.
48. Lalumiere RT (2014) Optogenetic dissection of amygdala functioning. Front Behav Neurosci 8:107.
49. Rosenfeld M, Brenner-Lavie H, Ari SG, Kavushansky A, Ben-Shachar D (2011) Perturbation in mitochondrial network dynamics and in complex I dependent cellular respiration in schizophrenia. Biol Psychiatry 69(10):980-988.
50. Brenner-Lavie H, et al. (2008) Dopamine modulates mitochondrial function in viable SH-SY5Y cells possibly via its interaction with complex I: Relevance to dopamine pathology in schizophrenia. Biochim Biophys Acta 1777(2):173-185.
51. Nestler EJ, Carlezon WA, Jr (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59(12):1151-1159.
52. Chaudhury D, et al. (2013) Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493(7433):532-536.
53. Stahl SM (2002) The psychopharmacology of energy and fatigue. J Clin Psychiatry 63(1):7-8.
54. Demyttenaere K, De Fruyt J, Stahl SM (2005) The many faces of fatigue in major depressive disorder. Int J Neuropsychopharmacol 8(1):93-105.
55. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443(7113):787-795.
56. Chang CC, Jou SH, Lin TT, Liu CS (2014) Mitochondrial DNA variation and increased oxidative damage in euthymic patients with bipolar disorder. Psychiatry Clin Neurosci 68(7):551-557.
57. Sandi C, Richter-Levin G (2009) From high anxiety trait to depression: A neurocognitive hypothesis. Trends Neurosci 32(6):312-320.
58. Castro JE, et al. (2012) Personality traits in rats predict vulnerability and resilience to developing stress-induced depression-like behaviors, HPA axis hyper-reactivity and brain changes in pERK1/2 activity. Psychoneuroendocrinology 37(8):1209-1223.
59. de Kloet ER, Joëls M, Holsboer F (2005) Stress and the brain: From adaptation to disease. Nat Rev Neurosci 6(6):463-475.
60. McEwen BS (2012) Brain on stress: How the social environment gets under the skin. Proc Natl Acad Sci USA 109(Suppl 2):17180-17185.