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Nicotine and Behavioral Markers of Risk for Schizophrenia: a Double-Blind, Placebo- Controlled, Cross-Over Study Lana Dépatie, M.Sc., Gillian A

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Nicotine and Behavioral Markers of Risk for Schizophrenia: a Double-Blind, Placebo- Controlled, Cross-Over Study Lana Dépatie, M.Sc., Gillian A Nicotine and Behavioral Markers of Risk for Schizophrenia: A Double-Blind, Placebo- Controlled, Cross-Over Study Lana Dépatie, M.Sc., Gillian A. O’Driscoll, Ph.D., Anne-Lise V. Holahan, B.Sc., Victoria Atkinson, R.N., Joseph X. Thavundayil, M.D., N. Ng Ying Kin, Ph.D., and Samarthji Lal, M.D. We investigated the effect of nicotine on three behavioral groups. A Drug ϫ Monitoring condition interaction (p Ͻ .01) markers of risk for schizophrenia: sustained attention on pursuit gain indicated that nicotine significantly (using the Continuous Performance Task (CPT)), increased pursuit gain in the no-monitoring condition in antisaccade performance, and smooth pursuit. Smooth patients and controls equally, but did not improve pursuit pursuit was investigated in two conditions, one in which in the monitoring condition. Thus, improvement in pursuit attention was enhanced (monitoring target changes) and may have been mediated via an effect on attention rather one in which attention was not enhanced (no monitoring). than by an effect on oculomotor function per se. In patients, Patients with schizophrenia (n ϭ 15) and controls (n ϭ 14) the magnitude of improvement in attention on nicotine was were given a 14-mg nicotine patch in a double-blind, correlated with the improvement on eye movement tasks. placebo-controlled, crossover design and plasma nicotine Thus, nicotine improves performance on both attention and concentrations were monitored. Nicotine concentrations oculomotor markers of risk for schizophrenia, possibly via were similar in both groups. A Group ϫ Drug interaction common mechanisms. (p Ͻ .02) on CPT hits indicated that nicotine improved [Neuropsychopharmacology 27:1056–1070, 2002] sustained attention in patients but not in controls. Nicotine © 2002 American College of Neuropsychopharmacology. significantly decreased antisaccade errors (p Ͻ .01) in both Published by Elsevier Science Inc. KEY WORDS: Nicotine; Schizophrenia; Sustained attention; Eye movements; Smooth pursuit; Antisaccade a high prevalence of smoking, higher than any other Nicotinic mechanisms have been implicated in the patho- psychiatric population (Hughes et al. 1986). It has been physiology of schizophrenia. Schizophrenic patients have postulated that schizophrenic patients may smoke as an attempt to self-medicate, that is, to correct a physiological deficit in nicotinic cholinergic mechanisms (Leonard et al. From the Department of Psychiatry (LD, GAO’D, SL) and Depart- 1996). Evidence in support of this interpretation include ment of Psychology (LD, GAO’D, A-LVH), McGill University, Mon- treal, and Douglas Hospital Research Centre, Verdun (LD, GAO’D, the findings that: (1) schizophrenic patients have fewer VA, JXT, NNYK, SL), Quebec, Canada. nicotinic receptors in post-mortem brain tissue than nor- Address correspondence to: Dr. Gillian A. O’Driscoll, Department mal smokers (Freedman et al. 1995; Breese et al. 2001); of Psychology, McGill University, Stewart Biological Sciences Building, 1205 Dr. Penfield Avenue, Montreal, Quebec, Canada, H3A 1B1. Tel.: (2) nicotine transiently normalizes sensory gating deficits (514) 398-4916; Fax: (514) 398-4896; E-mail: [email protected] among schizophrenic patients (Adler et al. 1993) and un- Received February 6, 2002; revised May 8, 2002; accepted May 9, affected first-degree relatives (Adler et al. 1992); and (3) 2002. Online publication: 5/10/02 at www.acnp.org/citations/ sensory gating deficits in schizophrenia have been Npp051002305. linked to an allele of chromosome 15, the gene locus for NEUROPSYCHOPHARMACOLOGY 2002–VOL. 27, NO. 6 © 2002 American College of Neuropsychopharmacology Published by Elsevier Science Inc. 0893-133X/02/$–see front matter 360 Park Avenue South, New York, NY 10010-1710 PII S0893-133X(02)00372-X NEUROPSYCHOPHARMACOLOGY 2002–VOL. 27, NO. 6 Nicotine and Markers of Risk for Schizophrenia 1057 a specific nicotinic receptor (i.e. ␣7-nicotinic receptor) controlled study of the effect of nicotine on sustained (Freedman et al. 1997). attention in schizophrenia (Levin et al. 1996). Family, twin and adoption studies have demon- The current study investigated the effect of nicotine strated that genetic factors play a major role in the etiol- on three putative markers of risk for schizophrenia, sus- ogy of schizophrenia (Bertelsen 1985; Gottesman et al. tained attention, antisaccade performance and smooth 1987; Kendler 1986). The risk for developing the illness pursuit eye movements using a double-blind, placebo- is increased among first-degree relatives of schizo- controlled, crossover design. Because schizophrenic pa- phrenic patients (Gottesman et al. 1987; Kety et al. 1994), tients have deficits on these tasks, and because there is and they can pass on vulnerability for schizophrenia evidence that they have abnormal nicotinic function, without having expressed the clinical disorder them- we hypothesized that nicotine would improve the per- selves (Gottesman and Bertelsen 1989). A subpopula- formance of patients to a greater extent than that of con- tion of schizophrenic patients’ first-degree relatives trols. Preliminary results from this study have been have cognitive or motor deficits similar to those ob- published in abstract form (O’Driscoll et al. 1999a; Dépatie served in affected probands (Adler et al. 1992; Levy et et al. 2001a,b). al. 1993; Cornblatt and Keilp 1994; Clementz et al. 1994). Thus, such deficits may be related to genetic vulnerabil- ity for schizophrenia (i.e., may be “behavioral markers SUBJECTS AND METHODS of risk” for the illness) (Holzman 1992). Subjects The data that Freedman and colleagues (1997) have provided implicating nicotine in the pathophysiology Twenty-nine smokers, 15 patients (3 women, 12 men) of schizophrenia suggest that nicotine is involved in the who met DSM-IV criteria (APA 1994) for schizophrenia pathophysiology of risk for the disorder as well. Specif- and 14 normal controls (3 women, 11 men) participated ically, sensory gating deficits which occur at elevated in the study. The two groups were highly similar both rates in relatives of schizophrenic patients are normalized demographically and in terms of nicotine dependence by nicotine (Adler et al. 1992) and are associated with an (Fagerström Test for Nicotine Dependence, FTND score) allele for a nicotinic receptor (Freedman et al. 1997). We (Fagerström 1978) (Table 1). were interested in the possibility that nicotinic mecha- Patients were recruited from the inpatient and out- nisms may be implicated as well in the pathophysiology patient population of the Douglas Hospital, Verdun, of other markers of risk for schizophrenia. Québec. DSM-IV diagnosis of schizophrenia was con- Abnormalities in sustained attention (Cornblatt and firmed through chart review. Current symptoms were Keilp 1994), antisaccade (Clementz et al. 1994), and rated using the Positive and Negative Syndrome Scale smooth pursuit (Levy et al. 1993) performance are all (PANSS) (Kay et al. 1987). Patients were found to have thought to be markers of risk for schizophrenia. Each an average score of 62.87 (Ϯ11.64). All patients were re- are found at elevated rates in schizophrenic patients ceiving neuroleptic treatment with an average dose of (Orzack and Kornetsky 1966; Holzman et al. 1973; Fukushima et al. 1990) their first-degree relatives (Levy et al. 1993; Cornblatt and Keilp 1994; Clementz et al. 1994) and other populations at high risk for the disor- Table 1. Demographic Characteristics der (Siever et al. 1984; Roitman et al. 1997; O’Driscoll et al. 1998), but at low rates in the general population. In Statistical addition, genetic studies suggest a significant hereditary Controls Patients Test P component to sustained attention (Cornblatt et al. 1988), No. of subjects 14 15 antisaccade performance (Myles-Worsley et al. 1999) and Age (yrs) 36.7 Ϯ 10.1 36.9 Ϯ 9.9 t(27) ϭ Ϫ.06 .95 smooth pursuit (Iacono and Lykken 1979; Bell et al. 1994). Nicotine has previously been shown to improve sus- Sex (% male) 80 79 ␹2(1) ϭ .008 .94 a Ϯ Ϯ ϭ Ϫ tained attention (Rusted and Warburton 1992; Warburton Father’s SES 3.7 2.4 4.2 2.1 t(25) .60 .55 Education (yrs) 13.4 Ϯ 3.0 11.4 Ϯ 3.1 t(27) ϭ 1.71 .10 and Arnall 1994; Levin et al. 1998) and smooth pursuit Full-scale IQ 102.1 Ϯ 15.7 95.2 Ϯ 7.7 t(24) ϭ 1.43 .17 performance (Domino et al. 1997) in normal controls, FTND (score)b 4.9 Ϯ 2.8 6.1 Ϯ 2.2 t(27) ϭ Ϫ1.30 .20 while the effect of nicotine on antisaccade performance Onset smoking has not been investigated. On sustained attention tasks, (age) 18.4 Ϯ 5.6 15.1 Ϯ 3.3 t(27) ϭ 1.91 .07 nicotine was found to increase accuracy and decrease Duration smoking (yrs) 18.13 Ϯ 11.1 21.8 Ϯ 10.0 t(27) ϭ Ϫ.88 .39 reaction time (Warburton and Mancuso 1998) as well as to prevent the decline in performance that occurs over time Data are presented as Mean Ϯ SD. (Frankenhaeuser et al. 1971). To date, no double-blind a SES ϭ socioeconomic status; father’s occupation ranked on an ordinal scale from 1 (major professional) to 9 (unemployed), from a modified studies of the effect of nicotine on oculomotor markers version of the Index of Social Status (Hollingshead and Redlich, 1958). of risk have been conducted and there has been only one b Fagerström Test for Nicotine Dependence (Fagerström, 1978). 1058 Lana Dépatie et al. NEUROPSYCHOPHARMACOLOGY 2002–VOL. 27, NO. 6 737.22 mg/day (Ϯ647.49 mg/day chlorpromazine for 1.5 h. The choice of time for administration of the equivalents) (Bezchlibnyk-Butler and Jeffries 1998). Six neurocognitive tests was based on the fact that plasma patients were receiving atypical neuroleptics (risperi- nicotine concentrations using the Nicoderm 14-mg done and/or olanzapine) and nine were receiving typical patch reach a plateau within 5.5 h after a single applica- neuroleptics. Eight of the patients were taking antimus- tion, and remain relatively constant for the ensuing 4 h carinic antiparkinsonian medication.
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