Unraveling the Contribution of Serotonergic Polymorphisms, Prefrontal Alpha Asymmetry, and Individual Alpha Peak Frequency to the Emotion-Related Impulsivity Endophenotype

Johnson SL, Tharp JA, Peckham AD et al (2017) A path model of different forms of impulsivity with externalizing and internalizing psychopathology: towards greater specificity. Br J Clin Psychol 56:235–252. https://doi.org/10.1111/bjc.12135 Carver CS, Johnson SL, Joormann J (2008) Serotonergic function, two-mode models of self-regulation, and vulnerability to depression: what depression has in common with impulsive aggression. Psychol Bull 134:912–943. https://doi.org/10.1037/a0013740 Swann AC, Anderson JC, Dougherty DM, Moeller FG (2001) Measurement of inter-episode impulsivity in bipolar disorder. Psychiatry Res 101:195–197. https://doi.org/10.1016/S0165-1781(00)00249-3 Guerrero MD, Barnes JD, Walsh JJ et al (2019) 24-hour movement behaviors and impulsivity. Pediatrics 144:e20190187. https://doi.org/10.1542/peds.2019-0187 Corruble E, Damy C, Guelfi JD (1999) Impulsivity: a relevant dimension in depression regarding suicide attempts? J Affect Disord 53:211–215. https://doi.org/10.1016/s0165-0327(98)00130-x Barratt E (1965) Factor analysis of some psychometric measures of impulsiveness and anxiety. Psychol Rep 16:547–554. https://doi.org/10.2466/pr0.1965.16.2.547 Dickman SJ (1990) Functional and dysfunctional impulsivity: personality and cognitive correlates. J Pers Soc Psychol 58:95–102. https://doi.org/10.1037/0022-3514.58.1.95 Whiteside SP, Lynam DR (2001) The Five Factor Model and impulsivity: using a structural model of personality to understand impulsivity. Pers Individ Dif 30:669–689. https://doi.org/10.1016/S0191-8869(00)00064-7 Carver CS, Johnson SL, Joormann J et al (2011) Serotonin transporter polymorphism interacts with childhood adversity to predict aspects of impulsivity. Psychol Sci 22:589–595. https://doi.org/10.1177/0956797611404085 Carver CS, Johnson SL, Kim Y (2016) Mu opioid receptor polymorphism, early social adversity, and social traits. Soc Neurosci 11:515–524. https://doi.org/10.1080/17470919.2015.1114965 Smith GT, Cyders MA (2016) Integrating affect and impulsivity: the role of positive and negative urgency in substance use risk. Drug Alcohol Depend 163:3–12. https://doi.org/10.1016/j.drugalcdep.2015.08.038 Dalley JW, Mar AC, Economidou D, Robbins TW (2008) Neurobehavioral mechanisms of impulsivity: fronto-striatal systems and functional neurochemistry. Pharmacol Biochem Behav 90:250–260. https://doi.org/10.1016/j.pbb.2007.12.021 Tricklebank MD, Daly E (2018) The serotonin system: history, neuropharmacology, and pathology, 1st Ed. London Academic Press (Elsevier) Canli T, Lesch KP (2007) Long story short: the serotonin transporter in emotion regulation and social cognition. Nat Neurosci 10:1103–1109. https://doi.org/10.1038/nn1964 Williams LM, Gatt JM, Kuan SA et al (2009) A polymorphism of the MAOA gene is associated with emotional brain markers and personality traits on an antisocial index. Neuropsychopharmacology 34:1797–1809. https://doi.org/10.1038/npp.2009.1 Iurescia S, Seripa D, Rinaldi M (2017) Looking beyond the 5-HTTLPR polymorphism: genetic and epigenetic layers of regulation affecting the serotonin transporter gene expression. Mol Neurobiol 54:8386–8403. https://doi.org/10.1007/s12035-016-0304-6 Niesler B, Kapeller J, Fell C et al (2010) 5-HTTLPR and STin2 polymorphisms in the serotonin transporter gene and irritable bowel syndrome: effect of bowel habit and sex. Eur J Gastroenterol Hepatol 22:856–861. https://doi.org/10.1097/MEG.0b013e32832e9d6b Kraft JB, Slager SL, McGrath PJ, Hamilton SP (2005) Sequence analysis of the serotonin transporter and associations with antidepressant response. Biol Psychiatry 58:374–381. https://doi.org/10.1016/j.biopsych.2005.04.048 Lesch K-P, Bengel D, Heils A et al (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 42:2482–2488. https://doi.org/10.1126/science.274.5292.1527 Oades RD, Lasky-Su J, Christiansen H et al (2008) The influence of serotonin-and other genes on impulsive behavioral aggression and cognitive impulsivity in children with attention-deficit/hyperactivity disorder (ADHD): findings from a family-based association test (FBAT) analysis. Behav Brain Funct 4:1–14. https://doi.org/10.1186/1744-9081-4-48 Evans J, Battersby S, Ogilvie AD et al (1997) Association of short alleles of a VNTR of the serotonin transporter gene with anxiety symptoms in patients presenting after deliberate self harm. Neuropharmacology 36:439–443. https://doi.org/10.1016/S0028-3908(97)00027-0 Ogilvie AD, Battersby S, Bubb VJ et al (1996) Polymorphism in serotonin transporter gene associated with susceptibility to major depression. Lancet 347:731–733. https://doi.org/10.1016/S0140-6736(96)90079-3 Bellivier F, Leroux M, Henry C et al (2002) Serotonin transporter gene polymorphism influences age at onset in patients with bipolar affective disorder. Neurosci Lett 334:17–20. https://doi.org/10.1016/S0304-3940(02)01029-7 De Lara CL, Dumais A, Rouleau G et al (2006) STin2 variant and family history of suicide as significant predictors of suicide completion in major depression. Biol Psychiatry 59:114–120. https://doi.org/10.1016/j.biopsych.2005.06.021 Rodríguez-Ramos Á, Antonio Moriana J, García-Torres F et al (2019) Emotional stability is associated with the MAOA promoter uVNTR polymorphism in women. Brain Behav 9:e01376. https://doi.org/10.1002/brb3.1376 Brunner HG, Nelen M, Breakefield XO et al (1993) Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 262:578–580. https://doi.org/10.1126/science.8211186 Furlong RA, Ho L, Rubinsztein JS et al (1999) Analysis of the monoamine oxidase A (MAOA) gene in bipolar affective disorder by association studies, meta-analyses, and sequencing of the promoter. Am J Med Genet Neuropsychiatr Genet 88:398–406. https://doi.org/10.1002/(SICI)1096-8628(19990820)88:4%3c398::AID-AJMG18%3e3.0.CO;2-Y Stetler DA, Davis C, Leavitt K et al (2014) Association of low-activity MAOA allelic variants with violent crime in incarcerated offenders. J Psychiatr Res 58:69–75. https://doi.org/10.1016/j.jpsychires.2014.07.006 Papousek I, Reiser EM, Schulter G et al (2013) Serotonin transporter genotype (5-HTTLPR) and electrocortical responses indicating the sensitivity to negative emotional cues. Emotion 13:1173–1181. https://doi.org/10.1037/a0033997 Rosadini G, Rossi GF (1967) On the suggested cerebral dominance for consciousness. Brain 90:101–112. https://doi.org/10.1093/brain/90.1.101 Gable PA, Neal LB, Threadgill AH (2018) Regulatory behavior and frontal activity: considering the role of revised-BIS in relative right frontal asymmetry. Psychophysiology 55:1–18. https://doi.org/10.1111/psyp.12910 Sutton SK, Davidson RJ (1997) Prefrontal brain asymmetry: a biological substrate of the behavioral approach and inhibition systems. Psychol Sci 8:204–210. https://doi.org/10.1111/j.1467-9280.1997.tb00413.x Tomarken AJ, Davidson RJ (1994) Frontal brain activation in repressors and nonrepressors. J Abnorm Psychol 103:339–349. https://doi.org/10.1037/0021-843X.103.2.339 Cyders MA, Zapolski TCB, Combs JL et al (2010) Experimental effect of positive urgency on negative outcomes from risk taking and on increased alcohol consumption. Psychol Addict Behav 24:367–375. https://doi.org/10.1037/A0019494 Zapolski TCB, Cyders MA, Smith GT (2009) Positive urgency predicts illegal drug use and risky sexual behavior. Psychol Addict Behav 23:348–354. https://doi.org/10.1037/A0014684 Pfurtscheller G, Stancák A, Neuper C (1996) Event-related synchronization (ERS) in the alpha band—an electrophysiological correlate of cortical idling: a review. Int J Psychophysiol 24:39–46. https://doi.org/10.1016/S0167-8760(96)00066-9 Harmon-Jones E, Gable PA, Peterson CK (2010) The role of asymmetric frontal cortical activity in emotion-related phenomena: a review and update. Biol Psychol 84:451–462. https://doi.org/10.1016/j.biopsycho.2009.08.010 Neal LB, Gable PA (2017) Regulatory control and impulsivity relate to resting frontal activity. Soc Cogn Affect Neurosci 12:1377–1383. https://doi.org/10.1093/scan/nsx080 Gable PA, Mechin NC, Hicks JA, Adams DL (2015) Supervisory control system and frontal asymmetry: neurophysiological traits of emotion-based impulsivity. Soc Cogn Affect Neurosci 10:1310–1315. https://doi.org/10.1093/scan/nsv017 Muhlert N, Lawrence AD (2015) Brain structure correlates of emotion-based rash impulsivity. Neuroimage 115:138–146. https://doi.org/10.1016/j.neuroimage.2015.04.061 Davidson RJ (2000) Affective style, psychopathology, and resilience: brain mechanisms and plasticity. Am Psychol 55:1196–1214. https://doi.org/10.1037/0003-066X.55.11.1196 Davidson RJ (2002) Anxiety and affective style: role of prefrontal cortex and amygdala. Biol Psychiatry 51:68–80. https://doi.org/10.1016/S0006-3223(01)01328-2 Jackson DC, Malmstadt JR, Larson CL, Davidson RJ (2000) Suppression and enhancement of emotional responses to unpleasant pictures. Psychophysiology 37:515–522. https://doi.org/10.1111/1469-8986.3740515 Ochsner KN, Bunge SA, Gross JJ, Gabrieli JDE (2002) Rethinking feelings: an fMRI study of the cognitive regulation of emotion. J Cogn Neurosci 14:1215–1229. https://doi.org/10.1162/089892902760807212 Anokhin AP, Van Baal GCM, Van Beijsterveldt CEM et al (2001) Genetic correlation between the P300 event-related brain potential and the EEG power spectrum. Behav Genet 31:545–554. https://doi.org/10.1023/A:1013341310865 Anokhin AP, Müller V, Lindenberger U et al (2006) Genetic influences on dynamic complexity of brain oscillations. Neurosci Lett 397:93–98. https://doi.org/10.1016/j.neulet.2005.12.025 Smit CM, Wright MJ, Hansell NK et al (2005) Genetic variation of individual alpha frequency (IAF) and alpha power in a large adolescent twin sample. Int J Psychophysiol 61:235–243. https://doi.org/10.1016/j.ijpsycho.2005.10.004 Gasser T, Bächer P, Steinberg H (1985) Test-retest reliability of spectral parameters of the EEG. Electroencephalogr Clin Neurophysiol 60:312–319. https://doi.org/10.1016/0013-4694(85)90005-7 Salinsky MC, Oken BS, Morehead L (1991) Test-retest reliability in EEG frequency analysis. Electroencephalogr Clin Neurophysiol 79:382–392. https://doi.org/10.1016/0013-4694(91)90203-G Grandy TH, Werkle-Bergner M, Chicherio C et al (2013) Peak individual alpha frequency qualifies as a stable neurophysiological trait marker in healthy younger and older adults. Psychophysiology 50:570–582. https://doi.org/10.1111/psyp.12043 Knyazev GG, Levin EA, Savostyanov AN (2008) Impulsivity, anxiety, and individual differences in evoked and induced brain oscillations. Int J Psychophysiol 68:242–254. https://doi.org/10.1016/j.ijpsycho.2008.02.010 Van Beijsterveldt CEM, Van Baal GCM (2002) Twin and family studies of the human electroencephalogram: a review and a meta-analysis. Biol Psychol 61:111–138. https://doi.org/10.1016/S0301-0511(02)00055-8 Javelle F, Bloch W, Knoop A et al (2021) Toward a neuroprotective shift: eight weeks of high intensity interval training reduces the neurotoxic kynurenine activity concurrently to impulsivity in emotionally impulsive humans—a randomized controlled trial. Brain Behav Immun. https://doi.org/10.1016/j.bbi.2021.04.020 Davies A, Rodriguez-Vicente AE, Austin G et al (2020) Serotonin re-uptake transporter gene polymorphisms are associated with imatinib-induced diarrhoea in chronic myeloid leukaemia patients - Supplementary material. Sci Rep 53:1689–1699. https://doi.org/10.1017/CBO9781107415324.004 Sabol SZ, Hu S, Hamer D (1998) A functional polymorphism in the monoamine oxidase A gene promoter. Hum Genet 103:273–279. https://doi.org/10.1007/s004390050816 Zhang H, Smith GN, Liu X, Holden JJ (2010) Association of MAOA, 5-HTT, and NET promoter polymorphisms with gene expression and protein activity in human placentas. Physiol Genomics 42:85–92. https://doi.org/10.1152/physiolgenomics.00220.2009 Auerbach RP, Stewart JG, Johnson SL (2017) Impulsivity and suicidality in adolescent inpatients. J Abnorm Child Psychol 45:91–103. https://doi.org/10.1007/s10802-016-0146-8 Carver CS, La VL, Kuhl J, Ganellen RJ (1988) Cognitive concomitants of depression: a further examination of the roles of generalization, high standards, and self-criticism. J Soc Clin Psychol 7:350–365. https://doi.org/10.1521/jscp.1988.7.4.350 Cyders MA, Smith GT, Spillane NS et al (2007) Integration of impulsivity and positive mood to predict risky behavior: development and validation of a measure of positive urgency. Psychol Assess 19:107–118. https://doi.org/10.1037/1040-3590.19.1.107 Javelle F, Wiegand M, Joormann J et al (2020) The German Three Factor Impulsivity Index: confirmatory factor analysis and ties to demographic and health-related variables. Pers Individ Dif 171:1–12. https://doi.org/10.1016/j.paid.2020.110470 Gramfort A (2013) MEG and EEG data analysis with MNE-Python. Front Neurosci 7:267. https://doi.org/10.3389/fnins.2013.00267 Bigdely-Shamlo N, Mullen T, Kothe C et al (2015) The PREP pipeline: standardized preprocessing for large-scale EEG analysis. Front Neuroinform 9:1–19. https://doi.org/10.3389/fninf.2015.00016 Harmon-Jones E, Allen JJB (1997) Behavioral activation sensitivity and resting frontal EEG asymmetry: covariation of putative indicators related to risk for mood disorders. J Abnorm Psychol 106:159–163. https://doi.org/10.1037/0021-843X.106.1.159 Porac C, Coren S (1981) Lateral preferences and human behavior. Lateral Prefer Hum Behav. https://doi.org/10.1007/978-1-4613-8139-6 Coan JA, Allen JJB, McKnight PE (2006) A capability model of individual differences in frontal EEG asymmetry. Biol Psychol 72:198. https://doi.org/10.1016/J.BIOPSYCHO.2005.10.003 Papousek I, Schulter G (2002) Covariations of EEG asymmetries and emotional states indicate that activity at frontopolar locations is particularly affected by state factors. Psychophysiology 39:350–360. https://doi.org/10.1017/S0048577201393083 Pivik RT, Broughton RJ, Coppola R et al (1993) Guidelines for the recording and quantitative analysis of electroencephalographic activity in research contexts. Psychophysiology 30:547–558. https://doi.org/10.1111/J.1469-8986.1993.TB02081.X Field A, Miles J, Field Z (2013) Discovering statistics using R, 4th Ed. SAGE Publications Ltd, Los Angeles | London | New Delhi | Singapore | Washington DC Eysenck SBG, Pearson PR, Easting G, Allsopp JF (1985) Age norms for impulsiveness, venturesomeness and empathy in adults. Pers Individ Dif 6:613–619. https://doi.org/10.1016/0191-8869(85)90011-X Madley-Dowd P, Hughes R, Tilling K, Heron J (2019) The proportion of missing data should not be used to guide decisions on multiple imputation. J Clin Epidemiol 110:63–73. https://doi.org/10.1016/J.JCLINEPI.2019.02.016 Dong Y, Peng CYJ (2013) Principled missing data methods for researchers. SpringerPlus 2:1–17. https://doi.org/10.1186/2193-1801-2-222/TABLES/3 Bowerman BL, O'Connell RT (1990) Linear statistical models : an applied approach, 2nd Ed. PWS-Kent Pub. Co, Boston Carver CS, Johnson SL, Timpano KR (2017) Toward a functional view of the p factor in psychopathology. Clin Psychol Sci 5:880–889. https://doi.org/10.1177/2167702617710037 Peters JR, Eisenlohr-Moul TA, Walsh EC, Derefinko KJ (2019) Exploring the pathophysiology of emotion-based impulsivity: the roles of the sympathetic nervous system and hostile reactivity. Psychiatry Res 267:368–375. https://doi.org/10.1016/j.psychres.2018.06.013 Hariri AR, Mattay VS, Tessitore A et al (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297:400–403. https://doi.org/10.1126/science.1071829 Pezawas L, Meyer-Lindenberg A, Drabant EM et al (2005) 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 8:828–834. https://doi.org/10.1038/nn1463 Lee BT, Ham BJ (2008) Monoamine oxidase A-uVNTR genotype affects limbic brain activity in response to affective facial stimuli. NeuroReport 19:515–519. https://doi.org/10.1097/WNR.0b013e3282f94294 Meyer-Lindenberg A, Buckholtz JW, Kolachana B et al (2006) Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Natl Acad Sci U S A 103:6269–6274. https://doi.org/10.1073/pnas.0511311103 Haegens S, Cousijn H, Wallis G et al (2014) Inter- and intra-individual variability in alpha peak frequency. Neuroimage 92:46–55. https://doi.org/10.1016/j.neuroimage.2014.01.049 Congdon E, Canli T (2005) The endophenotype of impulsivity: reaching consilience through behavioral, genetic, and neuroimaging approaches. Behav Cogn Neurosci Rev 4:262–281. https://doi.org/10.1177/1534582305285980 Yates JR, Darna M, Gipson CD et al (2015) Dissociable roles of dopamine and serotonin transporter function in a rat model of negative urgency. Behav Brain Res 291:201–208. https://doi.org/10.1016/j.bbr.2015.05.023 Javelle F, Li D, Zimmer P, Johnson SL (2019) Dietary intake of tryptophan tied emotion-related impulsivity in humans. Int J Vitam Nutr Res:1–8.https://doi.org/10.1024/0300-9831/a000608 Evenden JL (1999) Varieties of impulsivity. Psychopharmacology 146:348–361. https://doi.org/10.1007/PL00005481 Fairbanks LA, Melega WP, Jorgensen MJ et al (2001) Social impulsivity inversely associated with CSF 5-HIAA and fluoxetine exposure in vervet monkeys. Neuropsychopharmacology 24:370–378. https://doi.org/10.1016/S0893-133X(00)00211-6 Rodrigues J, Allen JJB, Müller M, Hewig J (2021) Methods matter: an examination of factors that moderate predictions of the capability model concerning the relationship of frontal asymmetry to trait measures. Biol Psychol 158:107993. https://doi.org/10.1016/J.BIOPSYCHO.2020.107993