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The Startle Reflex in Schizophrenia: Habituation and Personality Correlates

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The Startle Reflex in Schizophrenia: Habituation and Personality Correlates Schizophrenia Research 64 (2003) 165–173 www.elsevier.com/locate/schres The startle reflex in schizophrenia: habituation and personality correlates Sare J. Akdaga,b, Paul G. Nestora,b, Brian F. O’Donnellb,c, Margaret A. Niznikiewiczb, Martha E. Shentonb, Robert W. McCarleyb,* a Laboratory of Applied Neuropsychology, Department of Psychology, University of Massachusetts Boston, 100 Morrissey Boulevard, Boston, MA 02125, USA b Laboratory of Neuroscience, Department of Psychiatry, Harvard Medical School/Boston VA Healthcare System, Brockton Division, 116A, Brockton VAMC, 940 Belmont Street, Brockton, MA 02301, USA c Department of Psychology, Indiana University, Bloomington, IN 47405, USA Received 24 September 2002; received in revised form 10 February 2003; accepted 11 February 2003 Abstract Schizophrenia has long been associated with abnormal patterns of arousal that are thought to reflect disturbances in the reticular-activating system of the brain. Psychophysiological investigations of sensory responsivity have repeatedly demonstrated reduced reactivity and habituation to moderately intense stimuli in patients with schizophrenia. While not traditionally used as a measure of physiological arousal, the startle reflex represents an alternative method for studying reactivity and habituation in schizophrenia. This study examined eye blink responsivity to a repeatedly presented intense acoustic startle probe in men with chronic schizophrenia and healthy normal controls. Subjects’ personality profiles were also measured, as increased reactivity and arousal have been traditionally implicated as a physiological component to the personality trait of neuroticism. Results indicated that schizophrenic subjects did demonstrate significantly reduced rates of habituation to the acoustic startle probe and higher scores on measures of neuroticism in comparison to normal controls. However, no correlation between habituation rate and neuroticism emerged. These studies replicate previous findings of habituation in schizophrenia and provide further evidence for sensory reactivity disturbances in schizophrenia. The relationship of these findings to cognitive disturbances in schizophrenia is considered and directions for future research are discussed. D 2003 Elsevier Science B.V. All rights reserved. Keywords: Acoustic Startle; Habituation; Schizophrenia; Neuroticism; Arousal; Psychophysiology 1. Introduction 1966), which are thought to reflect disturbances in a well-described brain system ascending from the brain Schizophrenia has long been associated with stem to midbrain regions (Steriade, 1996). Psycho- abnormal patterns of arousal to stimuli (Venables, physiological studies primarily using EEG or skin conductance orienting response (SCOR) paradigms * Corresponding author. Tel.: +1-508-583-4500x2479; fax: +1- 508-586-0894. have consistently demonstrated higher resting rates E-mail address: robertÀmccarley@hms.harvard.edu of arousal, but lowered responsivity to orienting and (R.W. McCarley). other moderately intense stimuli in patients with 0920-9964/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0920-9964(03)00059-8 166 S.J. Akdag et al. / Schizophrenia Research 64 (2003) 165–173 schizophrenia (Venables, 1966; Venables and Wing, theory has shown that neurotic subjects demonstrate 1962; Dawson et al., 1992, 1994, Olbrich et al., 2001). more reactivity to negative stimuli than non-neurotic Consistent with these findings are studies that have subjects (Larsen and Ketelaar, 1991). demonstrated reduced autonomic habituation, as The current study uses the startle reflex paradigm assessed by electrodermal activity, to a repeatedly to further elucidate the nature and extent of habitu- presented sensory stimulus (e.g., Depue and Fowles, ation disturbances in schizophrenia and its relation- 1973; Gruzelier et al., 1981; Hollister et al., 1994). ship to personality traits. We first examine habituation These findings have demonstrated that schizophrenic rates of startle response in male patients compared to patients show irregular response patterns over time matched control subjects. Slower rates of habituation that result in slower rates of habituation. are predicted to characterize schizophrenic patients, Although not commonly used to quantify an organ- all of whom show a chronic disease course. In ism’s level of activation, the startle reflex is consid- addition, the personality trait of neuroticism will be ered a measure of reactivity to environmental stimuli, measured and correlated with startle response ampli- and as such follows a similar course of decreasing tudes for all subjects to examine the extent to which sensitivity to stimuli when repeatedly presented. habituation rates may relate to individual difference in Behaviorally, the startle reflex is best characterized personality profiles. as a sudden, involuntary reaction to an intense, unexpected sensory event that is characteristically manifested as a quick, involuntary eye blink (Lang 2. Methods et al., 1990). Animal studies of the startle response indicate that a primary brain stem circuit through the 2.1. Subjects nucleus reticularis pontis caudalis mediates the reflex (Davis, 1986; Cadenhead et al., 2000). The startle Twenty-three men with a DSM-IV diagnosis of reflex is most often measured using electromyo- schizophrenia were recruited from inpatient and out- graphic (EMG) technology to record the strength of patient populations of a Veterans Affairs Medical contraction of the orbicularis oculi muscle surround- Center. Seventeen normal controls were recruited via ing each eye as it blinks to the startle probe (Lang et newspaper advertisements from the communities sur- al., 1990). Studies of the startle response in schizo- rounding the medical center. Of the 40 subjects phrenia indicate a similar pattern of abnormal reac- recruited, 5 schizophrenic subjects and 1 normal tivity to that observed with autonomic measures, with control were excluded from final analyses due to schizophrenic subjects habituating more slowly than missing data and/or noncompliance with research non-schizophrenic psychiatric patients or normal con- protocol, leaving 18 schizophrenic patients and 16 trols (Geyer and Braff, 1982; Braff et al., 1992). normal controls. All subjects were screened for the Also of interest is that arousal has been consis- presence of active substance abuse, medical illnesses, tently implicated as a physiological component of neurological problems, and lifetime incidence of loss certain personality styles or profiles (Stelmack, of consciousness, all of which served as exclusion 1990; Gray, 1982; Larsen and Ketelaar, 1991), which criteria for this study. have demonstrated to be characteristic of schizophre- Before participation in the study, schizophrenic nia (DiLalla and Gottesman, 1995; Berenbaum and subjects’ psychiatric diagnoses were confirmed Fujita, 1994). In particular, the personality trait of through chart review and clinical interview with the neuroticism has been repeatedly associated with a Structured Clinical Interview for the Diagnostic and hypersensitivity to aversive sensory stimuli. Concep- Statistical Manual-Fourth Edition (SCID-IV) (First et tualized according to J.A. Gray’s model of a Behav- al., 1997). In addition, current symptom severity was ioral Inhibition System (BIS), neuroticism may be assessed using the Positive and Negative Syndrome thought of as a biologically based susceptibility to Scale (PANSS) (Kay et al., 1986). All schizophrenic negative stimuli that results in increased arousal and subjects in this study were medicated with an average negative affect in response to aversive or mismatched chlorpromazine (CPZ) equivalent dosage of 561.5 sensory events (Gray, 1982). Previous study of this mg/day (range 120–1333 mg/day; see Table 1). The S.J. Akdag et al. / Schizophrenia Research 64 (2003) 165–173 167 Table 1 phones that were plugged directly into the stimulus Demographic and descriptive statistics for SZ and control groups computer. Characteristic* SZ mean (S.D.) Control mean (S.D.) The eyeblink component of the startle response Age in years 41.6 ( F 7.9) 46.4 ( F 6.2) was measured by recording EMG activity from the Parental SES 2.7 ( F 1.1) 2.7 ( F 1.1) orbicularis oculi muscle beneath the left eye using 11- F F Mini-mental status 28.1 ( 1.7) 29.1 ( 1.4) mm Beckman Ag–AgCl miniature skin electrodes. CPZ in mg/day 561.5 ( F 401.7) N/A PANSS positive 17.1 ( F 7.1) N/A The reference, ground, and channel electrodes were syndrome score attached to subjects’ faces as suggested by Fridlund PANSS negative 18.1 ( F 5.7) N/A and Cacioppo (1986) with the ground electrode placed syndrome score in the center of the subject’s forehead and the refer- F PANSS general 35.7 ( 10.4) N/A ence and channel electrodes placed on the orbicularis syndrome score Length of illness 19.7 ( F 7.7) N/A oculi muscle parallel to the lower edge of the eyelid. Number of 7.5 ( F 3.5) N/A EMG activity was recorded at a bandpass range of hospitalizations 30–500 Hz using Neuroscan Synamps programmable Number of days 1624 ( F 3110) N/A digital amplifiers and acquisition software. EMG in hospital activity was then digitized at a 2-kHz rate for a sample *No significant difference between the two groups on matching interval of 100 ms prior and 600 ms after stimulus variables. onset. Editing of data using Neuroscan editing pro- grams included rectifying, filtering (0.01–20 Hz), and baseline correcting EMG activity. The amplitude of all average length of illness
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