Alexithymia influences brain activation during emotion perception but not regulation Jorien van der Velde, 1 Paula M. Gromann, 2 Marte Swart, 3 Durk Wiersma, 4 Lieuwe de Haan, 5 Richard Bruggeman, 4 Lydia Krabbendam, 2 and Andre ´ Aleman 1,6 1 Neuroimaging Center, University of Groningen, University Medical Center Groningen, 9713 AW Groningen, The Netherlands, 2 Department of Educational Neuroscience, Faculty of Psychology and Education, VU University Amsterdam, 1081 BT Amsterdam, The Netherlands, 3 Lentis, Center for Mental Healthcare, 9725 AG Groningen, The Netherlands, 4 Department of Psychiatry & Rob Giel Research Center, University Medical Center Groningen, 9713 GZ Groningen, The Netherlands, 5 Department of Psychiatry, Academic Medical Center Amsterdam, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands and 6 Department of Experimental Psychology, University of Groningen, 9712 TS Groningen, The Netherlands Alexithymia is a psychological construct that can be divided into a cognitive and affective dimension. The cognitive dimension is characterized by difficulties in identifying, verbalizing and analysing feelings. The affective dimension comprises reduced levels of emotional experience and imagination. Alexithymia is widely regarded to arise from an impairment of emotion regulation. This is the first functional magnetic resonance imaging (fMRI) study to critically evaluate this by investigating the neural correlates of emotion regulation as a function of alexithymia levels. The aim of the current study was to investigate the neural correlates underlying the two alexithymia dimensions during emotion perception and emotion regulation. Using fMRI, we scanned 51 healthy subjects while viewing, reappraising or suppressing negative emotional pictures. The results support the idea that cognitive alexithymia, but not affective alexithymia, is associated with lower activation in emotional attention and recognition networks during emotion perception. However, in contrast with several theories, no alexithymia-related differences were found during emotion regulation (neither reappraisal nor suppression). These findings suggest that alexithymia may result from an early emotion processing deficit rather than compromised frontal circuits subserving higher-order emotion regulation processes. Keywords: alexithymia; emotion processing; emotion regulation; amygdala; neuroimaging Alexithymia (‘no words for feelings’) is a psychological construct char- acterized by difficulties in identifying and describing one’s feelings, and in distinguishing them from bodily sensations of arousal. Individuals with high scores on alexithymia may further show a lack of imagin- ation and an externally oriented thinking style with a lack of intro- spection (Sifneos, 1973; Vorst and Bermond, 2001). Alexithymia can be divided into an affective and a cognitive dimension (Vorst and Bermond, 2001). The cognitive alexithymia dimension comprises the subscales difficulties in identifying, analysing and verbalizing feelings, while the affective dimension consists of the subscales emotionalizing (the degree to which someone is emotionally aroused by emotional stimuli) and fantasizing (the degree to which someone is inclined to imagine). Based on these dimensions, Bermond proposed to distin- guish two subtypes of alexithymia [Type I and Type II; (Bermond et al., 2007)]. Type I alexithymia is characterized by high scores on both dimensions (i.e. lower cognitive emotional processing capacities and lower emotional arousal). Type II is characterized by high scores on the cognitive dimension, but normal or even low scores on the affective dimension (i.e. lower cognitive emotional processing capaci- ties, but normal or heightened emotional arousal). Recent studies have suggested that the two alexithymia dimensions might be differently related to the development of psychopathology (Moormann et al., 2008; Van der Meer et al., 2009). Therefore, it is of relevance to gain insight into the neural bases underlying these two dimensions. Individuals with high scores on alexithymia experience difficulties in emotion processing. Furthermore, alexithymia is generally regarded to be an emotion regulation impairment (Taylor et al., 1997; Taylor and Bagby, 2004; Aleman, 2005; Wingbermu ¨hle et al., 2012). However, as far as we know, the neural correlates of emotion regulation in alex- ithymia through functional neuroimaging have not yet been investigated. Emotion processing can be seen as a three-phase process with (i) the identification of the emotional significance of a stimulus, (ii) the gen- eration of an affective state and (iii) emotion regulation (Phillips et al., 2003). Previous research has suggested that problems in emotion pro- cessing related to alexithymia may already occur during the first two phases of emotion processing. For example, individuals with high scores on alexithymia show deficits in the identification of facial ex- pressions (Swart et al., 2009; Grynberg et al., 2012) and declined at- tention towards emotional stimuli (Mueller et al., 2006). Furthermore, studies have indicated that individuals with high scores on alexithymia differ in their physiological responses to emotional stimuli (Roedema and Simons, 1999; Bermond et al., 2010), which might reflect differ- ences in the generation of affective states. Phillips and colleagues (2003) suggested that a ventral system, including the amygdala, insula, ventral striatum, ventral anterior cingulate cortex (ACC) and the ventral prefrontal cortex, is involved during the first two phases of emotion processing. Previous studies investigating alexithymia-related brain activation have reported activation differences in this system (Bermond et al., 2006; van der Velde et al., 2013). As far as we know, only one study examined the neural correlates of the two alex- ithymia dimensions separately through functional magnetic resonance imaging (fMRI) during emotion processing (Pouga et al., 2010), link- ing the cognitive dimension to lower amygdala activation and the Emotionalizing factor of the affective dimension to higher ACC and lower premotor activation. This indicates that the cognitive and affect- ive alexithymia dimensions may be associated with separable neural correlates during the first two phases of emotion processing. Received 14 October 2013; Revised 21 February 2014; Accepted 16 April 2014 Advance Access publication 23 April 2014 The GROUP study is supported by a grant from ZonMw, within the Mental Health programma (project number: 10.000.1002). A.A. is supported by a VICI grant from N.W.O., grant number 435-11-004. L.K. is supported in part by a VICI grant from N.W.O., grant number: 435-11-005. We would like to thank the families who invested time and effort to make the GROUP project possible. Furthermore, we would like to acknowledge Anita Sibeijn-Kuiper, Judith Streurman, Edith Liemburg and Michelle Servaas for their assistance with fMRI scanning and Dr Remco Renken for his advice regarding fMRI statistics. Correspondence should be addressed to Jorien van der Velde, Department of Neuroscience, Neuroimaging Center, UMCG-O&O, P.O. Box 196, 9700 AD Groningen, The Netherlands. E-mail: jorien.van.der.velde@umcg.nl doi:10.1093/scan/nsu056 SCAN (2015) 10, 285^293 ß The Author (2014). Published by Oxford University Press. For Permissions, please email: journals.permissions@oup.com by guest on April 19, 2016 http://scan.oxfordjournals.org/ Downloaded from