Elsevier

NeuroImage

Volume 54, Issue 3, 1 February 2011, Pages 2503-2513
NeuroImage

Cognitive versus automatic mechanisms of mood induction differentially activate left and right amygdala

https://doi.org/10.1016/j.neuroimage.2010.10.013Get rights and content

Abstract

The amygdala plays a key role in emotional processing. The specific contribution of the amygdala during the experience of one's own emotion, however, remains controversial and requires clarification. There is a long-standing debate on hemispheric lateralization of emotional processes, yet few studies to date directly investigated differential activation patterns for the left and right amygdala. Limited evidence supports right amygdala involvement in automatic processes of emotion and left amygdala involvement in conscious and cognitively controlled emotion processing. The present study investigated differential contributions of the left and right amygdala to cognitive and automatic mechanisms of mood induction. Using functional magnetic resonance imaging (fMRI), we examined hemispheric amygdala responses during two mood induction paradigms: a purely visual method presenting face stimuli and an audiovisual method using faces and music. Amygdala responses in 30 subjects (16 females) showed differences in lateralization patterns depending on the processing mode. The left amygdala exhibited comparable activation levels for both methods. The right amygdala, in contrast, showed increased activity only for the audiovisual condition and this activity was increasing over time. The left amygdala showed augmented activity with higher intensity ratings of negative emotional valence. These results support a left-lateralized cognitive and intentional control of mood and a right-sided more automatic induction of emotion that relies less on explicit reflection processes. The modulation of the left amygdala responses by subjective experience may reflect individual differences in the cognitive effort used to induce the mood. Thus, the central role of the amygdala may not be restricted to the perception of emotion in others but also extend into processes involved in regulation of mood.

Research Highlights

►Mood induction leads to differential lateralization patterns in the amygdala ►Right amygdala is more involved in automatic mechanisms of mood ►Left amygdala is more involved in cognitive and intentional control of mood ►Activity in left amygdala is modulated by subjective experience

Introduction

Humans experience a range of emotions each day. We receive a gift, see a friend suffer, or miss the bus. What happens in the brain when we experience these emotions? Until now, neurobiological research has focused on investigating how we perceive emotions expressed by others rather than how we experience i.e. feel our own emotions. For example, in experiments subjects were asked to label emotional expressions of faces, passively perceive faces while doing a low demanding cognitive task or only passively look at facial expressions (Costafreda et al., 2008, Fitzgerald et al., 2006, Fusar-Poli et al., 2009, Gur et al., 2002a, Yang et al., 2002). There are only few neuroimaging studies that examined the neural correlates of experiencing own emotions (Baumgartner et al., 2006b, Colibazzi et al., 2010, Habel et al., 2005, Mitterschiffthaler et al., 2007, Schneider et al., 1997). The majority of experimental investigations of emotional experiences relied on mood induction procedures. Most of these studies utilized visual stimuli, autobiographical memory recall or music to induce a specific mood. Colibazzi et al. (2010) for example presented emotionally evocative sentences and asked subjects to try to experience the emotion they would feel if the situation was real. Schneider et al. (1997) showed happy and sad facial expressions and instructed subjects to look at the faces and try to become happy/sad. Subjects were told that they could use autobiographical memory recall to support the mood induction. Still others played emotional music to subjects while they lay in the scanner and later asked them for emotional experiences during listening to the music (e.g. Koelsch et al., 2006, Mitterschiffthaler et al., 2007). These unimodal mood inductions require cognitive strategies to induce mood (Phillips et al., 2003). Teasdale et al. (1999) called this way of induction the cognitive route to emotion experience. However, Baumgartner et al. (2006b) suggested that the congruent presentation of emotional visual stimuli and music rather automatically evokes strong emotional feelings, deepens emotional experience and relies less on explicit reflection processes (Baumgartner et al., 2006b, Eldar et al., 2007, Mayer et al., 1995).

The amygdala is a key structure in the processing of emotion (for a review, see Sergerie et al., 2008). Previous mood induction studies suggest the amygdala as a structure that plays a central role in the generation and processing of emotional states (Barrett et al., 2007, Baumgartner et al., 2006b, Habel et al., 2005, Schneider et al., 1997). After presenting emotional sentences to subjects, Colibazzi et al. (2010) found that the amygdala was activated especially in response to highly arousing emotions. Researchers using the standardized mood induction involving the presentation of facial expressions combined with autobiographical memory recall found increased activation in mainly the left amygdala in response to sad and happy mood (Habel et al., 2005, Schneider et al., 1997). Other studies, in contrast, question the necessity of amygdala activation for the generation of subjective experience of emotions (Anderson and Phelps, 2002, Teasdale et al., 1999). Teasdale et al. (1999) did not find amygdala activation after induction of negative mood. Alike, Anderson and Phelps (2002) could show that patients with amygdala lesions report experiencing emotions very similar to healthy subjects. These divergent outcomes may be partly due to the heterogeneity of induction procedures. To our knowledge Baumgartner et al. (2006b) are the only authors to compare the neural correlates of visual and audiovisual mood induction procedures. In 9 subjects, the authors induced a negative mood in their subjects by presenting emotional pictures either with or without music played in the background. In comparison to the visual mood induction, the audiovisual condition yielded increased neural responses in the auditory cortices and in areas related to emotion processing such as the amygdala, hippocampus, parahippocampus, insula, striatum, medial ventral frontal cortex, cerebellum and fusiform gyrus. Amygdala activation was found only during the audiovisual but not during the visual mood induction. In the present study, we aim at further specifying the contribution of the amygdala to the experience of one's own emotions.

In spite of a longstanding debate regarding the hemispheric lateralization of emotions, few studies have investigated differences between right and left amygdala responses. There is limited evidence supporting a specific lateralization pattern of the amygdala (Markowitsch, 1998). It has been suggested that the right amygdala serves a relatively automatic and undifferentiated detection of emotional stimuli. Consequently, conditioned fear stimuli (Labar et al., 1998) and subliminally presented emotions (Morris et al., 1998) predominantly activated the right amygdala. The left amygdala, in contrast, is supposed to be more involved in intentional and cognitive processing of emotion. When subjects, for example, expected the presentation of fear stimuli beforehand, the left amygdala showed greater activation than the right (Phelps et al., 2001). Further support for this distinction comes from lesion studies. Glascher and Adolphs (2003) for example examined skin conductance responses (SCR) and emotional ratings in patients suffering from amygdala damage. Patients with lesions of the right amygdala had disturbed skin conductance responses in reaction to emotional stimuli but were able to discern different levels of arousal. Patients with left amygdala impairments, in contrast, showed intact SCRs but a significant reduction in arousal ratings. The authors concluded that the right amygdala mediates an automatic emotional reaction which is further differentiated by the left amygdala that discriminates differences in arousal magnitude. Funayama et al. (2001) published very similar findings for emotional startle responses.

The aim of the present study was to investigate differential contributions of the left and right amygdala to cognitive versus automatic mechanisms of emotion experience. We compared a visual mood induction with an audiovisual mood induction method that included music. Both mood induction methods primarily rely on cognitive strategies of mood induction. Based on the results of Baumgartner et al. (2006b), however, mood can be achieved with less explicit reflection processes during the audiovisual mood induction because the congruent presentation of visual and musical stimuli was shown to rather automatically facilitate the emotional experiences. We hypothesized that the left amygdala would be more active during the visual induction, while the right amygdala would show enhanced activation in the audiovisual condition. The emotional experience of both, happiness and sadness, evoked amygdala activation in previous studies (e.g. Habel et al., 2005). To probe both positive and negative affect, we investigated those two emotions in addition to a neutral condition.

For the evaluation of the success of a mood induction procedure, research mostly relied on subjective self-report. In addition to subjective self-report, we included an objective measure of mood to gain further support for effective mood induction. There is evidence that mood can alter attention (Raymond, 2009). Therefore, our subjects performed an attentional flanker task after the different mood inductions that was shown to be sensitive to mood in previous research (Willemssen et al., 2004).

A secondary objective of the present study was to examine the temporal pattern of amygdala activation. It has been demonstrated that amygdala activation habituates rapidly in response to repeated presentation of unpleasant pictures, faces, or complex visual stimuli (Fischer et al., 2000, Phillips et al., 2001, Wright et al., 2001). Mood, however, is a dynamic experience that develops and changes over time. Subjects do not only passively perceive emotional stimuli but actively attain and sustain a certain mood. Mood induction studies to date did not explicitly examine amygdala responses over time. Habel et al. (2004) reported the time course of amygdala activation in response to sad mood induction and the amygdala response did not decrease over the 60-s mood induction block. In the current study we directly examined patterns of amygdala activation over the time course of the mood induction. We hypothesized sustained or even increasing amygdala activation over the course of the mood induction.

Section snippets

Participants

Thirty healthy volunteers (16 females) with a mean age of 25.5 years (SD = 3.1) and a mean education of 13.6 years (SD = 1.7) participated in the study. All participants were right-handed as indicated by a minimal score of 6 on the Edinburgh Handedness Inventory (Oldfield, 1971). No subjects had a medical, neurological, or psychiatric illness as indicated by prior interview using the screening of the Structured Clinical Interview for DSM-IV, axis I disorders (SCID-I, German version, Wittchen et al.,

Behavioral results

The effectiveness of the mood induction procedure was confirmed by the repeated measures ANOVA revealing a significant main effect of emotion (F(2,58) = 141.2, p < 0.001; see Fig. 2). During sadness induction valence of self-perceived emotion was rated negative (mean: 2.12, SD = 0.58), during happiness induction valence was rated positive (mean = 4.07, SD = 0.48) and within the neutral conditions subjects reported neutral valence ratings (mean = 2.80, SD = 0.46). There was no significant effect of modality

Discussion

The current study showed that visual versus audiovisual mood induction techniques differentially activate left and right amygdala. Consistent with the hypothesis of left lateralization of cognitive strategies in the induction of emotions, amygdala activation was stronger in the left than in the right amygdala. The inclusion of music led to additional activity in the right but not in the left amygdala. Moreover, we observed an interaction between hemisphere, presentation modality, and time which

Acknowledgments

Funding for this study was provided by the German Research Foundation (DFG, IRTG 1328 and MA2631/4-1) and JARA Project “Realtime fMRI”. K.M. is a NARSAD Herman Foundation Investigator. R.G. and J.L. were supported by grants MH060722 and MH084856 from the National Institute of Mental Health. Further, we gratefully acknowledge the technical assistance of Cordula Kemper during the scanning as well as the participation of all our volunteers. Additional thanks to Thomas Baumgartner and Joset Etzel

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