Advertisement

Fear Conditioning and Affective Modulation of the Startle Reflex in Male Adolescents with Early-Onset or Adolescence-Onset Conduct Disorder and Healthy Control Subjects

Published:September 03, 2007DOI:https://doi.org/10.1016/j.biopsych.2007.06.019

      Background

      Impairments in emotional processing may play an etiological role in the development of aggressive or antisocial behavior such as is seen in conduct disorder (CD). These findings may be developmentally sensitive, with neuropsychological impairments confined to those with the early-onset form of CD, which emerges in childhood. We investigated whether adolescents with early- or adolescence-onset CD would acquire fear conditioned responses to a visual conditioned stimulus and show a normal pattern of affective modulation of the startle reflex.

      Methods

      Electrodermal activity was measured during the fear conditioning process, and electromyographic recording methods were used to assess blink magnitudes elicited by acoustic startle probes during the viewing of emotionally valenced pictures. Forty-one early-onset CD, 28 adolescence-onset CD, and 54 healthy control adolescents participated in the study.

      Results

      Both CD groups showed impaired differential fear conditioning relative to control subjects, while retaining the ability to generate normal skin conductance responses to the aversive unconditioned stimulus. There was a similar relationship between emotional valence of the slides and startle magnitude in CD and control adolescents, but startle-elicited blinks were lower across all emotion categories in both CD subtypes.

      Conclusions

      Fear conditioning deficits and reduced startle amplitudes were observed in participants with early- and adolescence-onset forms of CD. These findings are consistent with impairments in neural systems subserving emotion and involving the amygdala in CD, regardless of age of onset.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • American Psychiatric Association
        Diagnostic and Statistical Manual of Mental Disorders.
        4th ed. American Psychiatric Association, Washington, DC1994
        • Moffitt T.E.
        Adolescence-limited and life-course-persistent antisocial behavior: A developmental taxonomy.
        Psychol Rev. 1993; 100: 674-701
        • Van Goozen S.H.
        • Fairchild G.
        • Snoek H.
        • Harold G.T.
        The evidence for a neurobiological model of childhood antisocial behavior.
        Psychol Bull. 2007; 133: 149-182
        • Sterzer P.
        • Stadler C.
        • Krebs A.
        • Kleinschmidt A.
        • Poustka F.
        Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder.
        Biol Psychiatry. 2005; 57: 7-15
        • Everitt B.J.
        • Cardinal R.N.
        • Parkinson J.A.
        • Robbins T.W.
        Appetitive behavior: Impact of amygdala-dependent mechanisms of emotional learning.
        Ann N Y Acad Sci. 2003; 985: 233-250
        • Bechara A.
        • Tranel D.
        • Damasio H.
        • Adolphs R.
        • Rockland C.
        • Damasio A.R.
        Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans.
        Science. 1995; 269: 1115-1118
        • LaBar K.S.
        • LeDoux J.E.
        • Spencer D.D.
        • Phelps E.A.
        Impaired fear conditioning following unilateral temporal lobectomy in humans.
        J Neurosci. 1995; 15: 6846-6855
        • Büchel C.
        • Morris J.
        • Dolan R.J.
        • Friston K.J.
        Brain systems mediating aversive conditioning: An event-related fMRI study.
        Neuron. 1998; 20: 947-957
        • Van Goozen S.H.
        • Snoek H.
        • Matthys W.
        • Van Rossum I.
        • Van Engeland H.
        Evidence of fearlessness in behaviourally disordered children: A study on startle reflex modulation.
        J Child Psychol Psychiatry. 2004; 45: 884-892
        • Angold A.
        • Costello E.J.
        The epidemiology of disorders of conduct: Nosological issues and comorbidity.
        in: Hill J. Maughan B. Conduct Disorders in Childhood and Adolescence. Cambridge University Press, Cambridge, UK2001: 126-168
        • Levenston G.K.
        • Patrick C.J.
        • Bradley M.M.
        • Lang P.J.
        The psychopath as observer: Emotion and attention in picture processing.
        J Abnorm Psychol. 2000; 109: 373-385
        • Patrick C.J.
        • Bradley M.M.
        • Lang P.J.
        Emotion in the criminal psychopath: Startle reflex modulation.
        J Abnorm Psychol. 1993; 102: 82-92
        • Blair R.J.
        • Jones L.
        • Clark F.
        • Smith M.
        The psychopathic individual: A lack of responsiveness to distress cues?.
        Psychophysiology. 1997; 34: 192-198
        • Moffitt T.E.
        • Caspi A.
        • Harrington H.
        • Milne B.J.
        Males on the life-course persistent and adolescence-limited antisocial pathways: Follow-up at age 26 years.
        Dev Psychopathol. 2002; 14: 179-207
        • Kaufman J.
        • Birmaher B.
        • Brent D.
        • Rao U.
        • Flynn C.
        • Moreci P.
        • et al.
        Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data.
        J Am Acad Child Adolesc Psychiatry. 1997; 36: 980-988
        • Wechsler D.
        Wechsler Abbreviated Scale of Intelligence (WASI).
        Harcourt, San Antonio, TX1999
        • Bechara A.
        • Damasio H.
        Decision-making and addiction (part I): Impaired activation of somatic states in substance dependent individuals when pondering decisions with negative future consequences.
        Neuropsychologia. 2002; 40: 1675-1689
        • Lang P.J.
        • Bradley M.M.
        • Cuthbert B.N.
        International Affective Picture System (IAPS): Technical Manual and Affective Ratings.
        NIMH Center for the Study of Emotion and Attention, University of Florida, Gainsville, FL1997
        • Tassinary L.G.
        • Cacioppo J.T.
        The skeletomotor system: Surface electromyography.
        in: Cacioppo J.T. Tassinary L.G. Berntson G.G. Handbook of Psychophysiology. 2nd ed. Cambridge University Press, Cambridge, England2000: 163-199
        • Girden E.R.
        ANOVA: Repeated Measures.
        Sage, Newbury Park, CA1992
        • Herpertz S.C.
        • Werth U.
        • Lukas G.
        • Quanabi M.
        • Schuerkens A.
        • Kunert H.J.
        Emotion in criminal offenders with psychopathy and borderline personality disorder.
        Arch Gen Psychiatry. 2001; 58: 737-745
        • Cohen J.
        Statistical Power Analysis for the Behavioral Sciences.
        2nd ed. Erlbaum, Hillsdale, NJ1988
        • Hare R.D.
        • Quinn M.J.
        Psychopathy and autonomic conditioning.
        J Abnorm Psychol. 1971; 77: 223-235
        • Lykken D.T.
        A study of anxiety in the sociopathic personality.
        J Abnorm Psychol. 1957; 55: 6-10
        • Raine A.
        • Venables P.H.
        Classical conditioning and socialization–A biosocial interaction?.
        Pers Individ Dif. 1981; 2: 273-283
        • Raine A.
        • Venables P.H.
        • Williams M.
        Better autonomic conditioning and faster electrodermal half-recovery time at age 15 years as possible protective factors against crime at age 29 years.
        Dev Psychol. 1996; 32: 624-630
        • Birbaumer N.
        • Veit R.
        • Lotze M.
        • Erb M.
        • Hermann C.
        • Grodd W.
        • Flor H.
        Deficient fear conditioning in psychopathy: A functional magnetic resonance imaging study.
        Arch Gen Psychiatry. 2005; 62: 799-805
        • Angrilli A.
        • Mauri A.
        • Palomba D.
        • Flor H.
        • Birbaumer N.
        • Sartori G.
        • di Paola F.
        Startle reflex and emotion modulation impairment after a right amygdala lesion.
        Brain. 1996; 119: 1991-2000
        • Kettle J.W.
        • Andrewes D.G.
        • Allen N.B.
        Lateralization of the startle reflex circuit in humans: An examination with monaural probes following unilateral temporal lobe resection.
        Behav Neurosci. 2006; 120: 24-39
        • Buchanan T.W.
        • Tranel D.
        • Adolphs R.
        Anteromedial temporal lobe damage blocks startle modulation by fear and disgust.
        Behav Neurosci. 2004; 118: 429-437
        • Funayama E.S.
        • Grillon C.
        • Davis M.
        • Phelps E.
        A double dissociation in the affective modulation of startle in humans: Effects of unilateral temporal lobectomy.
        J Cogn Neurosci. 2001; 13: 721-729
        • Walker D.L.
        • Davis M.
        The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction.
        Pharmacol Biochem Behav. 2002; 71: 379-392
        • Hitchcock J.M.
        • Davis M.
        Efferent pathway of the amygdala involved in conditioned fear as measured with the fear-potentiated startle paradigm.
        Behav Neurosci. 1991; 105: 826-842
        • Robins L.N.
        Conduct disorder.
        J Child Psychol Psychiatry. 1991; 32: 193-212