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Neurophysiological Evidence of Cognitive Inhibition Anomalies in Persons with Major Depressive Disorder

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Neurophysiological Evidence of Cognitive Inhibition Anomalies in Persons with Major Depressive Disorder ARTICLE IN PRESS Clinical Neurophysiology xxx (2008) xxx–xxx www.elsevier.com/locate/clinph Neurophysiological evidence of cognitive inhibition anomalies in persons with major depressive disorder Heather E. McNeelya,b,*, Mark A. Laua,b,*, Bruce K. Christensena,b, Claude Alainc,d a Centre for Addiction and Mental Health, 250 College Street, Toronto, Ontario, Canada, M5T 1R8 b Department of Psychiatry, University of Toronto, Toronto, Ontario, Canada, M5T 1R8 c Rotman Research Institute, 3560 Bathurst Street, Toronto, Ontario, Canada, M6A 2E1 d Department of Psychology, University of Toronto, Toronto, Ontario, Canada, M5T 1R8 Accepted 19 March 2008 Abstract Objective: The neural correlates of inhibitory deficits for emotional semantic material in persons with major depressive disorder (MDD) were investigated. Methods: Individuals (n = 15) with a diagnosis of MDD or MDD in partial remission, and healthy controls (n = 14) underwent record- ing of event-related brain potentials (ERPs) while performing a computerized emotional Stroop task. Results: There were no group performance differences on the emotional Stroop task. However, the analysis of ERP waveforms revealed a larger negative wave peaking at about 170 ms over the left than the right hemisphere only in controls; a negative displacement (N450) at parietal sites for positive and negative words only for persons with MDD; in both groups, processing negative and positive words was associated with a positive displacement that peaked at about 450 ms and was larger over the left lateral frontal region; and, the N450 modulation correlated with negative automatic thinking and depressive symptoms. Conclusions: The electrophysiological data reveal early changes in neural activity associated with word processing as well as valence- related changes in the N450 component at parietal sites in MDD. Significance: This valence-related increase in N450 amplitude at parietal sites may reflect an automatic capture of attention by words with emotional valence. Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. Keywords: Depression; Event-related potentials; Cognitive inhibition; Emotional Stroop 1. Introduction Word Test (SCWT; Benoit et al., 1992; Everett et al., 1989; Lemelin et al., 1996); negative priming task (Linville, Depressed or dysphoric individuals demonstrate impair- 1996; MacQueen et al., 2000); dichotic listening paradigms ments on a variety of cognitive tasks that involve the inhi- (McCabe and Gotlib, 1993) and Continuous Performance bition of distracting elements such as the Stroop Colour Test (CPT; Buchsbaum et al., 1988; Goeleven et al., 2006). Many studies also point to a disproportionate impairment in depressed/dysphoric individuals’ ability to * Corresponding authors. Addresses: St. Joseph’s Healthcare, Hamilton, ignore distracting information when it is negatively valen- Centre for Mountain Health Services, 100 West 5th Street, Box 585, Suite ced (Goeleven et al., 2006; Gotlib et al., 2004, 2005; Lau E-223 H, Hamilton, Ont., Canada L8N 3K7. Tel.: +1 905 522 et al., 2007; Joormann, 2004; McCabe and Gotlib, 1993, 1155x36422; fax: +1 905 381 5635 (H.E. McNeely); BC Mental Health 1995; Segal et al., 1995). For example, the emotional & Addiction Services, 201-601 West Broadway, Vancouver, BC, Canada Stroop task has been widely used to measure the extent V5Z 4C2. Tel.: +1 604 707 6358; fax: +1 604 707 6399 (M.A. Lau). E-mail addresses: [email protected] (H.E. McNeely), to which persons can inhibit the automatic processing of [email protected] (M.A. Lau). depression-related words (Gotlib and McCann, 1984; Got- 1388-2457/$34.00 Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2008.03.031 Please cite this article in press as: McNeely HE et al., Neurophysiological evidence of cognitive inhibition anomalies ..., Clin Neu- rophysiol (2008), doi:10.1016/j.clinph.2008.03.031 ARTICLE IN PRESS 2 H.E. McNeely et al. / Clinical Neurophysiology xxx (2008) xxx–xxx lib and Cane, 1987; Segal and Vella, 1990; Segal et al., tion. In healthy individuals, one ERP modulation that 1995). In this paradigm, neutral, positive and negative has been shown to correlate with cognitive inhibition dur- words are shown in different ink colours. Participants must ing the standard Stroop colour-word task is the N450 wave ignore word meaning and name the ink colours as quickly (McNeely et al., 2003; Rebai et al., 1997; West and Alain, as possible. Depressed individuals are typically slower at 1999, 2000). The N450 reflects a phasic negativity over naming the ink colour of negative versus positive and neu- frontal and central scalp regions that peaks between 400 tral words, but there is generally no valence effect for and 500 ms after stimulus onset. It inverses in polarity over healthy controls. lateral and inferior frontal regions, and appears to arise Similarly, persons with Major Depressive Disorder from activity of the ACC (Liotti et al., 2000; McNeely (MDD) have shown difficulties in ignoring negative versus et al., 2003). The amplitude of the N450 is modulated by positive or neutral words embedded in a section of prose as the proportion of congruent to incongruent stimuli (West manifest by increased reading times (Lau et al., 2007). and Alain, 2000) and is significantly attenuated in persons Importantly, in this study, no performance deficits were with schizophrenia (McNeely et al., 2003) and older adults observed on the Stop Signal Task (Logan et al., 1997), a (West and Alain, 2000) indicating that it is sensitive to vari- measure of behavioural or motor response inhibition, sug- ations in cognitive control and inhibition. gesting that these deficits may be limited to the cognitive In the present study, we used a computerized emotional domain. Furthermore, valence-related increases in Stroop task to examine the effects of depression on behav- response times were not observed in a control group of ioural and electrophysiological indices of cognitive inhibi- individuals with mixed anxiety disorders, suggesting that tion for emotionally valenced semantic stimuli. Of most difficulties in inhibiting word valence were specific to interest in the behavioural data was the expected emotional depression and could not be accounted for by general psy- Stroop interference effect for negative trials, which would chopathology (Garber and Hollon, 1991). Importantly, be expressed as increased response latency and decreased prose reading time performance deficits were correlated accuracy. This was expected to occur selectively for nega- with increased negative cognition, as measured by the tive versus positive and neutral trials in individuals with Automatic Thoughts Questionnaire (Hollon and Kendall, depression relative to controls. Also, we expected to 1980); participants reporting the greatest degree of negative observe modulation of the N450 response associated with automatic thinking displayed the most difficulty inhibiting negative trials in persons with MDD, which would be task irrelevant, negative, emotional material. This finding is indicative of impaired neural processes underlying cogni- consistent with the hypothesis that disturbances of cogni- tive control deficits consistent with MDD. Finally, consis- tive control for affectively salient information may play a tent with Lau et al. (2007) we predicted that modulation of critical role in the preponderance of negative thinking in the N450 in participants with MDD would be correlated persons with MDD (Lau et al., 2007). with the increased frequency of negative automatic Cognition may serve an important role in the nexus thoughts. between clinical symptomatology and neurobiology as a more discrete, measurable, and easily manipulated interme- 2. Methods diary in psychopathology (Danion et al., 1996; Andreasen, 1997). Although few studies have been conducted to 2.1. Participants directly examine the links between specific behavioural or symptomatic features of MDD and neural abnormalities, Participants (ages 18–57 years) had normal or corrected- there is preliminary evidence to suggest that anomalies in to-normal vision, at least 12 years of formal education and the functioning of the anterior cingulate cortex (ACC) reported English as their primary language. Fifteen partic- may underlie MDD-related cognitive inhibitory dysfunc- ipants with depression (MDD, including four in partial tion. First, the ACC is an important component in the net- remission) were recruited from individuals seeking treat- work of structures implicated in the pathophysiology of ment at the Cognitive Behaviour Therapy (CBT) Unit at MDD (Lane et al., 1998; Mayberg, 1997; Mayberg et al., the Centre for Addiction and Mental Health, in Toronto, 1999). Second, research has demonstrated that the ACC Ontario, Canada or from the Toronto community through plays a fundamental role in cognitive inhibition among newspaper advertisements from August 2001 until August healthy individuals (see Bush et al., 2000, for a review). 2002. The Structured Clinical Interview for the DSM-IV In addition, in clinical populations (e.g., schizophrenia), Axis I disorders (SCID-I/P; First et al., 1998) was used observed inhibitory deficits are correlated with impaired to confirm a diagnosis of MDD and screen for co-morbid ACC function (Alain et al., 2002). Together, these lines diagnoses in the MDD group, and to exclude participants of evidence support a possible role for the ACC in inhibi-
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