Abstract
Rationale
Cigarette smokers smoke in part because nicotine helps regulate attention. Prepulse inhibition (PPI) of the startle reflex is a measure of early attentional gating that is reduced in abstinent smokers and in groups with attention regulation difficulties. Attention difficulties are found in people with posttraumatic stress disorder (PTSD).
Objectives
The aim of this study is to assess whether smoking and abstinence differentially affect the startle response and PPI in smokers with and without PTSD.
Methods
Startle response and PPI (prepulses at 60, 120, or 240 ms) were measured in smokers with (N = 39) and without (N = 61) PTSD, while smoking and again while abstinent.
Results
Participants with PTSD produced both larger magnitude and faster latency startle responses than controls. Across groups, PPI was greater when smoking than when abstinent. The PTSD and control group exhibited different patterns of PPI across prepulse intervals when smoking and when abstinent. Older age was associated with reduced PPI, but only when abstinent from smoking.
Conclusions
The effects of PTSD on startle magnitude and of smoking on PPI replicate earlier studies. The different pattern of PPI exhibited in PTSD and control groups across prepulse intervals, while smoking and abstinent suggests that previous research on smoking and PPI has been limited by not including longer prepulse intervals, and that nicotine may affect the time course as well as increasing the level of PPI. The reduced PPI among older participants during abstinence suggests that nicotine may play a role in maintaining attention in older smokers, which may motivate continued smoking in older individuals.
Similar content being viewed by others
References
American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association, Washington
Ashare R, Hawk L Jr (2012) Effects of smoking abstinence on impulsive behavior among smokers high and low in ADHD-like symptoms. Psychopharmacol 219:537–547
Bakshi V, Alsene K, Roseboom P, Conners E (2007) Enduring sensorimotor gating abnormalities following predator exposure or corticotrophin-releasing factor in rats: a model for PTSD-like information-processing deficits? Neuropharmacology 62:737–748
Beckham JC, Roodman AA, Shipley RH, Hertzberg MA, Cunha GH, Kudler HS, Levin ED, Rose JE, Fairbank JA (1995) Smoking in Vietnam combat veterans with posttraumatic stress disorder. J Trauma Stress 8:461–472
Beckham JC, Kirby AC, Feldman ME, Hertzberg MA, Moore SD, Crawford AL, Davidson JRT, Fairbank JA (1997) Prevalence and correlates of heavy smoking in Vietnam veterans with chronic posttraumatic stress disorder. Addict Behav 22:637–647
Beckham J, Moore S, Feldman M, Kirby A, Hertzberg M, Fairbank J (1998) Self-report and physician-rated health in combat veterans with posttraumatic stress disorder. Am J Psychiatry 155:1565–1569
Beckham JC, Feldman ME, Vrana SR, Mozley SL, Erkanli A, Clancy CP, Rose JE (2005) Immediate antecedents of cigarette smoking in smokers with and without posttraumatic stress disorder: a preliminary study. Exp Clin Psychopharmacol 13:218–228
Beckham JC, Dennis MF, McClernon FJ, Mozley SL, Collie CF, Vrana SR (2007) The effects of cigarette smoking on script-driven imagery in smokers with and without posttraumatic stress disorder. Addict Behav 32:2900–2915
Beckham JC, Calhoun PS, Dennis MF, Wilson SM, Johnson YC, Dedert EA (2012) Predictors of lapse in the first week of smoking abstinence in posttraumatic stress disorder and non-posttraumatic stress disorder smokers. Nicotine Tob Res Epub ahead of print [Nov. 2012]
Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS, Keane TM (1995) The development of a clinician-administered posttraumatic stress disorder scale. J Trauma Stress 8:75–80
Bradley M, Cuthbert B, Lang P (1993) Pictures as prepulse: attention and emotion in startle modification. Psychophysiology 30:541–545
Braff DL, Geyer MA (1990) Sensorimotor gating and schizophrenia: human and animal model studies. Arch Gen Psychiatry 47:181–188
Braff DL, Geyer MA, Swerdlow N (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacol 156:234–258
Bushnell PJ, Levin ED, Marrocco RT, Sarter MF, Strupp BJ, Warburton DM (2000) Attention as a target of intoxication: insights and methods from studies of drug abuse. Neurotoxicol Teratol 22:487–502
Butler RW, Braff DL, Rausch J, Jenkins MA, Sprock J, Geyer MA (1990) Physiological evidence of exaggerated startle response in a subgroup of Vietnam veterans with combat-related posttraumatic stress disorder. Am J Psychiatry 147:1308–1312
Della Casa V, Hofer I, Weiner I, Feldon J (1998) The effects of smoking on acoustic prepulse inhibition in healthy men and women. Psychopharmacol 137:362–368
Duncan E, Madonick S, Chakravorty S, Parwani A, Szilagyi S, Efferen T, Gonzenbach S, Angrist B, Rotrosen J (2001) Effects of smoking on acoustic startle and prepulse inhibition in humans. Psychopharmacol 156:266–272
Ellwanger J, Geyer M, Braff D (2003) The relationship of age to prepulse inhibition and habituation of the acoustic startle response. Biol Psychol 62:175–195
First MB, Spitzer RL, Gibbon M, Williams JBW (1994) Structured Clinical Interview for Axis I DSM-IV Disorders. Biometrics Research Department, New York
George T, Termine A, Sacco K, Allen T, Reutenauer E, Vessicchio J, Duncan E (2006) A preliminary study of the effects of cigarette smoking on prepulse inhibition in schizophrenia: involvement of nicotinic receptor mechanisms. Schizophr Res 87:307–315
Graham F (1975) The more or less startling effects of weak prestimuli. Psychophysiology 12:238–248
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, Morgan CA, Southwick SM, Davison M, Charney DS (1996) Baseline startle amplitude and prepulse inhibition in Vietnam veterans with posttraumatic stress disorder. Psychiatr Res 64:169–178
Grillon C, Morgan C, Davis M, Southwick S (1998a) Effect of darkness on acoustic startle in Vietnam veterans with PTSD. Am J Psychiatry 155:812–817
Grillon C, Morgan CA, Davis M, Southwick SM (1998b) Effects of experimental context and explicit threat cues on acoustic startle in Vietnam veterans with posttraumatic stress disorder. Biol Psychiatr 44:1027–1036
Heishman SJ (1998) What aspects of human performance are truly enhanced by nicotine? Addiction 93:317–320
Heishman SJ (1999) Behavioral and cognitive effects of smoking: relationship to nicotine addiction. Nicotine Tob Res 1(suppl 2):S143–S147
Holstein D, Vollenweider F, Jäncke L, Schopper C, Csomor P (2010) P50 suppression, prepulse inhibition, and startle reactivity in the same patient cohort suffering from posttraumatic stress disorder. J Affect Disord 126:188–197
Hutchinson K, Niaura R, Swift R (2000) The effects of smoking high nicotine cigarettes on prepulse inhibition, startle latency, and subjective responses. Psychopharmacol 150:244–252
Jovanovic T, Norrholm S, Sakoman A, Esterajher S, Kozaric-Kovacic D (2009) Altered resting psychophysiology and startle response in Croatian combat veterans with PTSD. Int J Psychophysiol 71:264–268
Kassel JD, Stroud LR, Paronis CA (2003) Smoking, stress, and negative affect: correlation, causation, and context across stages of smoking. Psychol Bull 129:270–304
Kleykamp BA, Heishman SJ (2011) The older smoker. J Am Med Assoc 306:876–877
Kohl S, Heekeren K, Klosterkotter J, Kuhn J (2013) Prepulse inhibition in psychiatric disorders—apart from schizophrenia. J Psychiatr Res 47:445–452
Kok A (2000) Age-related changes in involuntary and voluntary attention as reflected in components of the event-related potential (ERP). Biol Psychol 54:107–143
Kubany ES, Haynes SN, Leisen MB, Owens JA, Kaplan AS, Watson SB, Burns K (2000) Development and preliminary validation of a brief broad-spectrum measure of trauma exposure: The Traumatic Life Events Questionnaire. Psychol Assess 12:210–224
Kumari V, Gray JA (1999) Smoking withdrawal, nicotine dependence, and prepulse inhibition of the acoustic startle reflex. Psychopharmacol 141:11–15
Kumari V, Checkley W, Gray JA (1996) Effect of cigarette smoking on prepulse inhibition of the acoustic startle reflex in healthy male smokers. Psychopharmacol 128:54–60
Kumari V, Cotter PA, Checkley SA, Gray JA (1997) Effect of acute subcutaneous nicotine on prepulse inhibition of the acoustic startle inhibition of the acoustic startle reflex in healthy male nonsmokers. Psychopharmacol 132:389–395
Kumari V, Soni W, Sharma T (2001) Influence of cigarette smoking on prepulse inhibition of the acoustic startle response in schizophrenia. Hum Psychopharmacol Clin Exp 16:321–326
Lando HA, McCovern PG, Barrios FX (1990) Comparative evaluation of American Cancer Society and American Lung Association smoking cessation clinics. Am J Public Health 80:554–559
Lasser K, Boyd JW, Woolhander S, Himmelstein DU, McCormick D, Bor DH (2000) Smoking and mental illness: a population-based prevalence study. JAMA 284:2606–2610
Levin ED, Wilson W, Rose JE, McEvoy J (1996) Nicotine–haloperidol interactions and cognitive performance in schizophrenics. Neuropsychopharmacology 15:429–436
Lipschitz DS, Mayes LM, Rasmusson AM, Anyan W, Billingslea E, Gueorguieva R, Southwick SM (2005) Baseline and modulated acoustic startle response in adolescent girls with posttraumatic stress disorder. J Am Acad Child Adolesc Psychiatry 44:807–814
Ludewig K, Ludewig S, Seitz A, Obrist M, Geyer M, Vollenweider F (2003) The acoustic startle reflex and its modulation: effects of age and gender in humans. Biol Psychol 63:311–323
Ornitz EM, Pynoos RS (1989) Startle modulation in children with posttraumatic stress disorder. Am J Psychiatry 146:866–870
Pole N (2007) The psychophysiology of posttraumatic stress disorder: a meta-analysis. Psychol Bull 133:725–746
Postma P, Kumari V, Sharma T, Hines M, Gray JA (2001) Startle response during smoking and 24 h after withdrawal predicts successful smoking cessation. Psychopharmacol 156:360–367
Postma P, Gray JA, Sharma T, Geyer M, Mehrotra R, Das M, Zachariah E, Hines M, Williams SCR, Kumari V (2006) A behavioral and functional neuroimaging investigation into the effects of nicotine on sensorimotor gating in healthy subjects and persons with schizophrenia. Psychopharmacol 184:189–199
Rose JE, Behm FM (2004) Extinguishing the rewarding value of smoke cues: pharmacologic and behavioral treatments. Nicotine Tob Res 6:523–532
Swerdlow N, Hartman PL, Auerbach PP (1997) Changes in sensorimotor inhibition across the menstrual cycle: implications for neuropsychiatric disorders. Biol Psychiatr 41:452–460
Swerdlow N, Geyer M, Hartman P, Sprock J, Auerback P, Cadenhead K, Perry W, Braff D (1999) Sex differences in sensorimotor gating of the human startle reflex: all smoke? Psychopharmacol 146:228–232
Vasterling JJ, Brailey K, Constans JI, Sutker PB (1998) Attention and memory dysfunction in posttraumatic stress disorder. Neuropsychology 12:125–133
Vrana SR, Spence EL, Lang PJ (1988) The startle probe response: a new measure of emotion? J Abnorm Psychol 97:487–491
Woznica A, Sacco K, George T (2009) Prepulse inhibition deficits in schizophrenia are modified by smoking status. Schizophr Res 112:86–90
Acknowledgments
This work was supported primarily by the National Institutes of Health grants 2R01CA081595, 2K24DA016388 and the Department of Veterans Affairs Office of Research and Development, Clinical Science. We would like to thank the participants who volunteered to participate in this study. The authors also wish to thank Terry Blumenthal for consultation on scoring and interpreting the startle response and PPI results. The views expressed in this presentation are those of the authors and do not necessarily represent the views of the Department of Veterans Affairs or the National Institutes of Health.
Conflict of interest
The authors have no competing interests to report.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vrana, S.R., Calhoun, P.S., McClernon, F.J. et al. Effects of smoking on the acoustic startle response and prepulse inhibition in smokers with and without posttraumatic stress disorder. Psychopharmacology 230, 477–485 (2013). https://doi.org/10.1007/s00213-013-3181-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00213-013-3181-y