The Modulation of the Startle Reflex as Predictor of Alcohol Use Disorders in a Sample of Heavy Drinkers: A 4-Year Follow-Up Study
Rosa Jurado-Barba
Research Institute Hospital 12 de Octubre (i + 12), Madrid, Spain
Camilo José Cela University , Madrid, Spain
Search for more papers by this authorCorresponding Author
Almudena Duque
Pontifical University of Salamanca , Salamanca, Spain
Complutense University of Madrid , Madrid, Spain
Reprint requests: Almudena Duque, PhD, Pontifical University of Salamanca, C/ Compañía, 5, Salamanca, Spain; Tel.: +1-34-923-277 100 Ext: 7615; Fax: + 1-34-923-277-114; E-mail: [email protected]Search for more papers by this authorJosé Ramón López-Trabada
University Hospital 12 de Octubre , Madrid, Spain
Search for more papers by this authorIsabel Martínez-Gras
University Hospital 12 de Octubre , Madrid, Spain
Biomedical Research Center Network for Mental Health (CIBERSAM) , Madrid, Spain
Search for more papers by this authorMaría Salud García-Gutiérrez
Instituto de Neurociencias , Miguel Hernández University, San Juan de Alicante, Alicante, Spain
Red Temática de Investigación Cooperativa en Salud (RETICS) , Red de Trastornos Adictivos, Instituto de Salud Carlos III, MICINN and FEDER, Madrid, Spain
Search for more papers by this authorFrancisco Navarrete
Instituto de Neurociencias , Miguel Hernández University, San Juan de Alicante, Alicante, Spain
Red Temática de Investigación Cooperativa en Salud (RETICS) , Red de Trastornos Adictivos, Instituto de Salud Carlos III, MICINN and FEDER, Madrid, Spain
Search for more papers by this authorFrancisco López-Muñoz
Camilo José Cela University , Madrid, Spain
Search for more papers by this authorMiguel Ángel Jiménez-Arriero
Research Institute Hospital 12 de Octubre (i + 12), Madrid, Spain
University Hospital 12 de Octubre , Madrid, Spain
Biomedical Research Center Network for Mental Health (CIBERSAM) , Madrid, Spain
Search for more papers by this authorJorge Manzanares
Instituto de Neurociencias , Miguel Hernández University, San Juan de Alicante, Alicante, Spain
Red Temática de Investigación Cooperativa en Salud (RETICS) , Red de Trastornos Adictivos, Instituto de Salud Carlos III, MICINN and FEDER, Madrid, Spain
Search for more papers by this authorGabriel Rubio
Complutense University of Madrid , Madrid, Spain
University Hospital 12 de Octubre , Madrid, Spain
Red Temática de Investigación Cooperativa en Salud (RETICS) , Red de Trastornos Adictivos, Instituto de Salud Carlos III, MICINN and FEDER, Madrid, Spain
Search for more papers by this authorRosa Jurado-Barba
Research Institute Hospital 12 de Octubre (i + 12), Madrid, Spain
Camilo José Cela University , Madrid, Spain
Search for more papers by this authorCorresponding Author
Almudena Duque
Pontifical University of Salamanca , Salamanca, Spain
Complutense University of Madrid , Madrid, Spain
Reprint requests: Almudena Duque, PhD, Pontifical University of Salamanca, C/ Compañía, 5, Salamanca, Spain; Tel.: +1-34-923-277 100 Ext: 7615; Fax: + 1-34-923-277-114; E-mail: [email protected]Search for more papers by this authorJosé Ramón López-Trabada
University Hospital 12 de Octubre , Madrid, Spain
Search for more papers by this authorIsabel Martínez-Gras
University Hospital 12 de Octubre , Madrid, Spain
Biomedical Research Center Network for Mental Health (CIBERSAM) , Madrid, Spain
Search for more papers by this authorMaría Salud García-Gutiérrez
Instituto de Neurociencias , Miguel Hernández University, San Juan de Alicante, Alicante, Spain
Red Temática de Investigación Cooperativa en Salud (RETICS) , Red de Trastornos Adictivos, Instituto de Salud Carlos III, MICINN and FEDER, Madrid, Spain
Search for more papers by this authorFrancisco Navarrete
Instituto de Neurociencias , Miguel Hernández University, San Juan de Alicante, Alicante, Spain
Red Temática de Investigación Cooperativa en Salud (RETICS) , Red de Trastornos Adictivos, Instituto de Salud Carlos III, MICINN and FEDER, Madrid, Spain
Search for more papers by this authorFrancisco López-Muñoz
Camilo José Cela University , Madrid, Spain
Search for more papers by this authorMiguel Ángel Jiménez-Arriero
Research Institute Hospital 12 de Octubre (i + 12), Madrid, Spain
University Hospital 12 de Octubre , Madrid, Spain
Biomedical Research Center Network for Mental Health (CIBERSAM) , Madrid, Spain
Search for more papers by this authorJorge Manzanares
Instituto de Neurociencias , Miguel Hernández University, San Juan de Alicante, Alicante, Spain
Red Temática de Investigación Cooperativa en Salud (RETICS) , Red de Trastornos Adictivos, Instituto de Salud Carlos III, MICINN and FEDER, Madrid, Spain
Search for more papers by this authorGabriel Rubio
Complutense University of Madrid , Madrid, Spain
University Hospital 12 de Octubre , Madrid, Spain
Red Temática de Investigación Cooperativa en Salud (RETICS) , Red de Trastornos Adictivos, Instituto de Salud Carlos III, MICINN and FEDER, Madrid, Spain
Search for more papers by this authorAbstract
Background
Previous studies demonstrated that patients with alcohol use disorders (AUDs) show altered startle reflex responses to alcohol-related stimuli. However, there is little information about the role of these altered responses in the development of AUDs. This study examined the startle reflex response to different visual stimuli and the role of these patterns in the development of AUDs in a 4-year follow-up.
Methods
Two hundred and thirty-nine (nondependent) heavy-drinking participants were selected. In the baseline period, the startle reflex responses to alcohol-related, aversive, appetitive, and neutral pictures were assessed. Startle reflex responses to these pictures were used as predictive variables. Status drinking (alcohol dependence and nondependence) assessed at 4-year follow-up was used as outcome measure.
Results
At the 4-year follow-up assessment, 46% of participants fulfilled DSM-IV alcohol abuse or dependence criteria. Alcohol dependence status was predicted by an attenuated startle reflex response to alcohol-related and aversive pictures.
Conclusions
This study revealed that an attenuated modulation of startle reflex response to alcohol-related and aversive stimuli could be used as a clinical marker to predict the development of AUDs in participants with previous alcohol consumption.
Graphical Abstract
The participants are 239 men with a heavy-drinking profile who had not received previous formal treatment for Alcohol Use Disorder (AUD). Results show that in comparison with participants remaining as heavy drinkers and remitted at 4-year follow-up, alcohol-dependent subjects show an attenuated startle reflex response to alcohol-related, aversive, appetitive and neutral pictures. The predictive analysis shows that the startle reflex response to alcohol-related and aversive pictures are significant predictors of alcohol-dependence status at the follow-up 4 years later.
References
- Alonso J, Angermeyer MC, Bernert R, Bruffaerts TS; ESEMeD/MHEDEA (2000) Investigators (2004) Use of mental health services in Europe: results from the European Study of the Epidemiology of Mental Disorders (ESEMeD) project. Acta Psychiatr Scand 109: 47–54.
- Bradley MM, Cuthbert BN, Lang PJ (1993) Pictures as prepulse: attention and emotion in startle modification. Psychophysiology 30: 541–545.
- Cacioppo JT, Gardner WL, Berntson GG (1999) The affect system has parallel and integrative processing components: form follows function. J Pers Soc Psychol 76: 839–855.
- Campbell BA, Wood G, McBride T (1997) Origins of orienting and defensive responses: an evolutionary perspective, in Attention and Orienting: Sensory and Motivational Processes ( PJ Lang, RF Simons, M Balaban eds), pp 41–67. Erlbaum, Hillsdale, NJ.
- Carroll CA, Vohs JL, O'donnell BF, Shekhar A, Hetrick WP (2007) Sensorimotor gating in manic and mixed episode bipolar disorder. Bipolar Disord 9: 221–229.
- Caseras FX, Fullana MA, Riba J, Barbanoj MJ, Aluja A, Torrubia R (2006) Influence of individual differences in the behavioral inhibition system and stimulus content (fear versus blood-disgust) on affective startle reflex modulation. Biol Psychol 72: 251–256.
- Conti LH, Printz MP (2003) Rat strain-dependent effects of repeated stress on the acoustic startle response. Behav Brain Res 144: 11–18.
- Corr PJ, Wilson GD, Fotiadou M, Kumari V, Gray NS, Checkley SA, Gray JA (1995) Personality and affective modulation of the startle reflex. Person Individ Diff 19: 543–553.
- Curtin JJ, Lang AR, Patrick CJ, Stritzke WG (1998) Alcohol and fear-potentiated startle: the role of competing cognitive demands in the stress-reducing effects of intoxication. J Abnorm Psychol 107: 547–557.
- Dawson ME, Hazlett EA, Filion DL, Nuechterlein KH, Schell AM (1993) Attention and schizophrenia: impaired modulation of the startle reflex. J Abnorm Psychol 102: 633–641.
- Drobes D, Carter A, Goldman M (2009) Alcohol expectancies and reactivity to alcohol-related and affective cues. Exp Clin Psychoparhamacol 17: 1–9.
- First MB, Spitzer R, Gibbon M, Williams JBW (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. (SCID-I/P). New York: Biometrics Research, New York State Psychiatric Institute.
- Giakoumaki SG, Bitsios P, Frangou S, Roussos P, Aasen I, Galea A, Kumari V (2010) Low baseline startle and deficient affective startle modulation in remitted bipolar disorder patients and their unaffected siblings. Psychophysiology 47: 659–668.
- Gonzales M, Garrett C, Chapman CD, Dess NK (2008) Stress-induced attenuation of acoustic startle in low-saccharin-consuming rats. Biol Psychol 79: 193–199.
- Gray JA (1987) The Psychology of Fear and Stress. Cambridge University Press, Cambridge.
- Grillon C (2002) Startle reactivity and anxiety disorders: aversive conditioning, context, and neurobiology. Biol Psychiatry 52: 958–975.
- Grillon C, Baas J (2003) A review of the modulation of the startle reflex by affective states and its application in psychiatry. Clin Neurophysiol 114: 1557–1579.
- Grillon C, Dierker L, Merikangas KR (1998) Fear-potentiated startle in adolescent offspring of parents with anxiety disorders. Biol Psychiatry 44: 990–997.
- Grusser SM, Heinz A, Flor H (2000) Standardized stimuli to assess drug craving and drug memory in addicts. J Neural Transm 107: 715–720.
- Grusser SM, Heinz A, Raabe A, Wessa M, Podschus J, Flor H (2002) Stimulus-induced craving and startle potentiation in abstinent alcoholics and controls. Eur Psychiatry 17: 188–193.
- Heinz A, Lober S, Georgi A, Wrase J, Hermann D, Rey ER, Wellek S, Mann K (2003) Reward craving and withdrawal relief craving: assessment of different motivational pathways to alcohol intake. Alcohol Alcohol 38: 35–39.
- Jovanovic T, Szilagyi S, Chakravorty S, Fiallos AM, Lewison BJ, Parwani A, Schwartz MP, Gonzenbach S, Rotrosen JP, Duncan EJ (2004) Menstrual cycle phase effects on prepulse inhibition of acoustic startle. Psychophysiology 41: 401–406.
- Kaviani H, Gray JA, Checkley SA, Raven PW, Wilson GD, Kumari V (2004) Affective modulation of the startle response in depression: influence of the severity of depression, anhedonia, and anxiety. J Affect Disord 83: 21–31.
- Kujawa A, Glenn CR, Hajcak G, Klein DN (2015) Affective modulation of the startle response among children at high and low risk for anxiety disorders. Psychol Med 45: 2647–2656.
- Kumari V, Kaviani H, Raven PW, Gray JA, Checkley SA (2001) Enhanced startle reaction to acoustic stimuli in patients with obsessive-compulsive disorder. Am J Psychiatry 158: 134–136.
- Lang PJ, Bradley MM, Cuthbert BN (1990) Emotion, attention, and the startle reflex. Psychol Rev 97: 377–395.
- Lang PJ, Bradley MM, Cuthbert BN (1997) Motivated attention: affect, activation and action, in Attention and Orienting: Sensory and Motivational Processes ( PJ Lang, RF Simons, M Balaban eds), pp 119–137. Erlbaum, Hillsdale, NJ.
- Lang PJ, Bradley MM, Cuthbert BN (2005) International Affective Picture System (IAPS). Affective Ratings of Pictures and Instruction Manual. Technical Report no. A-6. The Center for Research in Psychophysiology, University of Florida.
- Lang PJ, McTeague LM, Bradley MM (2014) Pathological anxiety and function/dysfunction in the brain's fear/defense circuitry. Restor Neurol Neurosci 32: 63–77.
- Leménager T, Hill H, Reinhard I, Hoffmann S, Zimmermann US, Hermann D, Smolka MN, Kiefer F, Vollstädt-Klein S, Heinz A, Mann K (2014) Association between alcohol-cue modulated startle reactions and drinking behaviour in alcohol dependent patients – results of the PREDICT study. Int J Psychophysiol 94: 263–271.
- Levenston GK, Patrick CJ, Bradley MM, Lang PJ (2000) The psychopath as observer: emotion and attention in picture processing. J Abnorm Psychol 109: 373–385.
- Loeber S, Croissant B, Nakovics H, Zimmer A, Georgi A, Klein S, Diener C, Heinz A, Mann K, Flor H (2007) The startle reflex in alcohol-dependent patients: changes after cognitive-behavioral therapy and predictive validity for drinking behavior – a pilot study. Psychother Psychosom 76: 385–390.
- Maisto SA, Sobell MB, Cooper AM, Sobell LC (1979) Test-retest reliability of retrospective self-reports in three populations of alcohol abusers. J Behav Assess 1: 315–326.
10.1007/BF01321373 Google Scholar
- Mann K, Gordon J, McLeod A (2009) Reflection and reflective practice in health professions education: a systematic review. Adv Health Sci Educ Theory Pract 14: 595–621.
- McTeague LM, Lang PJ (2012) The anxiety spectrum and the reflex physiology of defense: from circumscribed fear to broad distress. Depress Anxiety 29: 264–281.
- Moltó JMS, Poy R, Segarra P, Partor MC, Tormo MP (1999) Un Nuevo método para el estudio experimental de las emociones: El International Affective Picture System (IAPS). Adaptación española. Revista de Psicología Aplicada 52: 55–87.
- Mucha RF, Geier A, Stuhlinger M, Mundle G (2000) Appetitive effects of drug cues modelled by pictures of the intake ritual: generality of cue-modulated startle examined with inpatient alcoholics. Psychopharmacology 151: 428–432.
- Patrick CJ, Bradley MM, Lang PJ (1993) Emotion in the criminal psychopath: startle reflex modulation. J Abnorm Psychol 102: 82–92.
- Piasecki TM, Robertson BM, Epler AJ (2010) Hangover and risk for alcohol use disorders: existing evidence and potential mechanisms. Curr Drug Abuse Rev 3: 92–102.
- Poli E, Angrilli A (2015) Greater general startle reflex is associated with greater anxiety levels: a correlational study on 111 young women. Front Behav Neurosci 9: 1–6.
- Rehm J, Allamani A, Aubin HJ, Della Vedova R, Elekes Z, Frick U, Jakubczyk A, Kostogianni N, Landsmane I, Manthey J, Miquel L, Paille F, Pieper L, Probst C, Scafuri F, Shield KD, Snikere S, Struzzo P, Trapencieris M, Voller F, Wittchen HU, Gual A, Wojnar M (2014) People with alcohol use disorders in specialized care in eight different European countries. Alcohol Alcohol 50: 310–318.
- Rehm J, Anderson P, Barry J, Dimitrov P, Elekes Z, Feijão F, Frick U, Gual A, Kraus L, Marmet S, Raninen J, Rehm MX, Scafato E, Shield KD, Trapencieris M, Gmel G (2015) Prevalence of and potential influencing factors for alcohol dependence in Europe. Eur Addict Res 21: 6–18.
- Rehm J, Shield KD, Gmel G, Rehm MX, Frick U (2013) Modelling the impact of alcohol dependence in mortality burden and the effect of available treatment interventions in the European Union. Eur Neuropsychopharmacol 23: 89–97.
- Rehm J, Shield KD, Rehm MX, Gmel G (2012) Frick U (2012) Alcohol Consumption, Alcohol Dependence, and Attributable Burden of Disease in Europe: Potential Gains from Effective Interventions for Alcohol Dependence. CAMH, Toronto, ON.
- Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 18: 247–291.
- Rubio G, Borrell J, Jiménez M, Jurado R, Gruesser SM, Heinz A (2013) Variables involved in the cue modulation of the startle reflex in alcohol-dependent patients. Addict Biol 18: 170–180.
- Rubio G, Urosa B, Santo-Domingo J (1998) Validación de la escala de la intensidad de la dependencia alcohólica (EIDA). Psiquiatría Biológica 1: 44–47.
- Saladin ME, Drobes DJ, Coffey SF, Libet JM (2002) The human startle reflex and alcohol cue reactivity: effects of early versus late abstinence. Psychol Addict Behav 16: 98–105.
- Samokhvalov AV, Popova S, Room R, Rehm J (2010) Disability associated with alcohol abuse and dependence. Alcohol Clin Exp Res 34: 1871–1878.
- Selye H (1950) Stress and the general adaptation syndrome. BMJ 17: 1384–1392.
- Sobell LC, Maisto SA, Sobell MB, Cooper AM (1979) Reliability of alcohol abusers’ self-reports of drinking behavior. Behav Res Ther 17: 157–160.
- Vila JSM, Ramirez I, Fernández MC, Cobos P, Rodríguez S (2001) El Sistema Internacional de Imágenes Afectivas (IAPS). Adaptación española. Revista de Psicología Aplicada 54: 635–657.
- Waters AM, Nazarian M, Mineka S, Zinbarg RE, Griffith JW, Naliboff B, Ornitza EM, Crascke MG (2014) Context and explicit threat cue modulation of the startle reflex: preliminary evidence of distinctions between adolescents with principal fear disorders versus distress disorders. Psychiatry Res 217: 93–99.
- Zimmermann U, Spring K, Kunz-Ebrecht SR, Uhr M, Wittchen HU, Holsboer F (2004) Effect of ethanol on hypothalamic-pituitary-adrenal system response to psychosocial stress in sons of alcohol-dependent fathers. Neuropsychopharmacology 29: 1156–1165.