Elsevier

Neuropsychologia

Volume 49, Issue 10, August 2011, Pages 2947-2956
Neuropsychologia

Emotional self-reference: Brain structures involved in the processing of words describing one's own emotions

https://doi.org/10.1016/j.neuropsychologia.2011.06.026Get rights and content

Abstract

The present functional magnetic resonance imaging study investigated the role of emotion-related (e.g., amygdala) and self-related brain structures (MPFC in particular) in the processing of emotional words varying in stimulus reference. Healthy subjects (N = 22) were presented with emotional (pleasant or unpleasant) or neutral words in three different conditions: (1) self (e.g., my fear), (2) other (e.g., his fear) and (3) no reference (e.g., the fear). Processing of unpleasant words was associated with increased amygdala and also insula activation across all conditions. Pleasant stimuli were specifically associated with increased activation of amygdala and insula when related to the self (vs. other and no reference). Activity in the MPFC (vMPFC in particular) and anterior cingulate cortex (ACC) was preferentially increased during processing of self-related emotional words (vs. other and no reference). These results demonstrate that amygdala activation in response to emotional stimuli is modulated by stimulus reference and that brain structures implicated in emotional and self-related processing might be important for the subjective experience of one's own emotions.

Highlights

► Healthy participants read emotion words varying in self-reference. ► Emotion words were related to the self, the other or had no self-other reference. ► Brain activity was investigated by means of functional imaging methods. ► Processing of emotion words increased amygdala and insula activity. ► MPFC (vMPFC and ACC) were activated specifically for self-related emotion words.

Introduction

Emotion and the self are two fascinating research topics. Ever since William James, researchers have sought answers to the questions what constitutes emotions and the self and how both phenomena might interact. Although no clear theoretical consensus has yet been reached, contemporary empirical research converges on the view that both, emotion and the self, are neurally grounded phenomena (Damasio, 1994, Damasio, 1999), and associated with activity changes in specific brain regions. Regarding emotions, neuroimaging studies have been successful in tracing the brain circuitry underlying the processing of emotional stimuli. One robust finding of this research is that processing of emotional stimuli leads to enhanced activity in the amygdala. This could be demonstrated for different stimulus materials, including high arousing pictures, faces (Zald, 2003, for reviews) as well as more symbolic stimuli such as emotionally arousing words (e.g., Cunningham et al., 2004, Hamann and Mao, 2002, Herbert et al., 2009, Tabert et al., 2001). Although the amygdala responds rapidly to emotional information this does not mean that the subjects themselves actually experience fear or any emotion at all when looking at a photograph of a fearful face, or while reading an emotionally challenging word. In general emotions can be characterized as adaptive response patterns of an organism, associated with changes in the body and the brain, that are elicited instantaneously in the presence of emotionally significant external or internal events that promote or challenge the organisms survival and well-being (Russell, 2003, Scherer, 2005). These response patterns and concomitant changes in the body and the brain need not be consciously aware to the subject (Craig, 2008, Damasio, 1994, Damasio, 1999). Feelings might result from emotions, however in contrast to emotions, feelings refer to the subjective and conscious experience of emotions (e.g., Barrett et al., 2007a, Damasio, 1994, Damasio, 1999).

Lesion studies suggest that the amygdala is involved in more basic emotional processing, but not necessarily in conscious emotion processing and the generation of feelings (e.g., Adolphs et al., 1994, Anderson and Phelps, 2002; for reviews see Adolphs, 2002). The amygdala is an emotion detection structure (Damasio, 1994, Damasio, 1999, LeDoux, 1996, Öhman and Mineka, 2001). It ensures reflexive responding to stimuli that challenge or protect individual survival and well-being. Activation of the amygdala might therefore also change, and/or increase in intensity during processing of personally relevant emotional stimuli (Adolphs et al., 1998, Cristinzio et al., 2011, N’Diaye et al., 2010, Modinos et al., 2009, Rameson et al., 2010, Yoshimura et al., 2009). This would be in line with the suggestion that the amygdala responds to a broad range of stimuli of emotional significance and of subjective emotional relevance (Sander, Grandjean, & Scherer, 2005).

Regarding the self, several neuroimaging studies demonstrate specific brain regions to be more active when individuals engage in self-referential processing tasks like judging stimuli (e.g., trait adjectives) in terms of their personal relatedness or self-descriptiveness (Craik et al., 1999, Kelley et al., 2002, Zysset et al., 2003; for review see Northoff et al., 2006). Subcomponents of this so called cortical midline structures (CMS) comprise, in particular, the medial prefrontal cortex (MPFC), and, amongst others, the posterior cingulate cortex (PCC) and the inferior parietal cortex (e.g., the precuneus) (for reviews on CMS see Northoff & Bermpohl, 2004). Several studies report changes in activity in regions of the CMS during active emotional modulation tasks. Most of these studies used tasks, in which participants were explicitly instructed to evaluate the emotional stimuli for their self-descriptiveness, their personal relevance (e.g., like me vs. not like me), or from a first relative to a third person perspective (e.g., Fossati et al., 2003, Gusnard et al., 2001, Moran et al., 2006; for an overview see Lee & Siegle, 2009). Other tasks employed in these studies used active emotion regulation conditions during which participants actively regulated their responses to emotional stimuli by reappraising their meaning with regard to the implications for themselves (e.g., Ochsner et al., 2002, Ochsner et al., 2004a, Ochsner et al., 2004b).

One emerging point of evidence from these studies is that reflection upon the own emotional state enhances activity in the medial prefrontal cortex (MPFC). The MPFC is interconnected with dorsal prefrontal cortex, the anterior cingulate cortex (ACC) and the insular cortex and receives in- and output from limbic emotion structures such as the amygdala (Fuster, 2008), thus providing a converging zone for the integration of information about interoceptive sensations, cognitive and emotional states. Notably the ventral MPFC (vMPFC) is more engaged in the evaluation of own emotions compared to, for instance, the emotions of others or a control condition (e.g., passive viewing). The dorsal MPFC (dMPFC), in contrast, appears to be related to self-referential processing in general (Schmitz & Johnson, 2007). Models based on meta-analytical data regarding emotion and the self (Northoff and Bermpohl, 2004, Schmitz and Johnson, 2007) suggest two different medial prefrontal sub-systems: The first system primarily comprises the vMPFC, the anterior cingulate (ACC), amygdala and insula. This sub-system is hypothesized to be responsible for the online evaluation of incoming emotional information as self-relevant. The second sub-system, including the dMPFC, precuneus and posterior cingulate cortex, is supposed to enable a more detailed stimulus analysis based on self-reflection either in conjunction with or independent of the former sub-system. Up to now, it remains unclear if changes in activity in one or both of these MPFC systems can be stimulated by self-related emotional stimuli in the absence of presented self-reflective processing instructions.

Research on embodied cognition (e.g., Barrett and Lindquist, 2008, Barrett et al., 2007b), as well as traditional semantic network models of emotion and cognition (Bower, 1981, Lang, 1979) suggest that processing of emotional content encompasses links to all aspects of its perceptual properties, its usage and emotional connotations. Thus, the word fear, for example, not only represents the concept of fear, but includes links to the word's purpose, operations and physiological consequences, possibly reinstating feelings of pleasure/displeasure and arousal even in the absence of a concrete emotion eliciting external event. This has also been highlighted by emotion models stating the relevance of the representation of actual and reactivated bodily experiences (Craig, 2002, Craig, 2009, Damasio, 1994, Damasio, 1999). Reading verbal expressions describing own emotions might thus automatically arouse and activate the amygdala, and additionally direct the reader's attention towards the monitoring of internal, mental and bodily states and the evaluation of emotional experience from current and past experience.

Previous research suggest that both the vMPFC, the insula and the ACC are key structures associated with subjective awareness of inner bodily states (interoception) and the representation and regulation of subjective emotional experience (Barrett et al., 2007a, Craig, 2002, Craig, 2009, Lane, 2000, Paulus and Frank, 2003, Zysset et al., 2003). Accordingly, one would expect activity in the amygdala, insula but also the MPFC (vMPFC in particular) and the ACC to be more active during processing of words related the own emotion compared to a control condition of passive viewing of emotion words that contain no particular reference or are related to another person.

Building upon and extending previous research the present study aimed, for the first time, to directly investigate this hypothesis by measuring brain activity underlying the processing of one's own emotions without confounding effects related to a specific task at hand. To this end, healthy participants underwent functional imaging while they read silently a series of verbal expressions that described either own emotions, the emotions of another person or contained no self-other reference at all.

Section snippets

Participants

Twenty-two healthy, right-handed native speakers of German (eight males, fourteen females; mean age: 23.5 years, SD = 2.7) without history of drug abuse, chronic bodily or neurological and psychiatric diseases, or medication for any of these participated in the fMRI experiment. All participants scored normally on self-report measures of mood (M = 3.3; SD = 2.5) (BDI, Hautzinger, Bailer, Worall, & Keller, 1194), and also state (M = 35.7; SD = 5.3) and trait anxiety (M = 36.3; SD = 5.8) (STAI, Laux, Glanzmann,

Effects of emotion, unreferenced

Activity in the left amygdala as well as the right insula was significantly enhanced during reading of unpleasant compared to neutral nouns that contained no self-other reference (Table 1a). For pleasant nouns, there was no difference in amygdala or insula activity compared to neutral nouns. Also, there was a significant increase in activity in occipital, parietal as well as temporal brain regions during reading of emotional (unpleasant and unpleasant) compared to neutral nouns (Table 1b).

Effects of self-reference on emotion processing

Discussion

The present study demonstrates how variations in stimulus reference (related to the self, vs. the other, vs. no particular reference) associated with emotion words influence brain activity patterns in emotion-related and self-related brain structures in a silent reading task. During reading, processing of unpleasant words compared to neutral and pleasant words increased amygdala and insula activation regardless of the stimuli's reference (self, other, no reference). This is consistent with

Acknowledgements

This research study was supported by the German Research Foundation (DFG).

We thank the reviewers and the Editor Daniel T. Tranel for their helpful comments on our manuscript.

References (74)

  • D. Sander et al.

    A systems approach to appraisal mechanisms in emotion

    Neural Networks

    (2005)
  • T.W. Schmitz et al.

    Relevance to self: A brief review and framework of neural systems underlying appraisal

    Neuroscience Biobehavioral Reviews

    (2007)
  • M.H. Tabert et al.

    Differential amygdala activation during emotional decision and recognition memory tasks using unpleasant words: An fMRI study

    Neuropsychologia

    (2001)
  • N. Tzourio-Mazoyer et al.

    Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain

    Neuroimage

    (2002)
  • S. Yoshimura et al.

    Self-referential processing of negative stimuli within the ventral anterior cingulate gyrus and right amygdala

    Brain and Cognition

    (2009)
  • D.H. Zald

    The human amygdala and the emotional evaluation of sensory stimuli

    Brain Research

    (2003)
  • S. Zysset et al.

    Functional specialization within the anterior medial prefrontal cortex: A functional magnetic resonance imaging study with human subjects

    Neuroscience Letters

    (2003)
  • R. Adolphs

    Recognizing emotion from facial expressions: Psychological and neurological mechanisms

    Behavioral and Cognitive Neuroscience Reviews

    (2002)
  • R. Adolphs et al.

    Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala

    Nature

    (1994)
  • R. Adolphs et al.

    The human amygdala in social judgment

    Nature

    (1998)
  • S. Anders et al.

    Brain activity underlying emotional valence and arousal: A response-related fMRI study

    Human Brain Mapping

    (2004)
  • A.K. Anderson

    Feeling emotional: The amygdala links emotional perception and experience

    Social Cognitive and Affective Neuroscience

    (2007)
  • A.K. Anderson et al.

    Is the human amygdala critical for the subjective experience of emotion? Evidence of intact dispositional affect in patients with amygdale lesions

    Journal of Cognitive Neuroscience

    (2002)
  • R.H. Baayen et al.

    The CELEX lexical database (CD-ROM). Linguistic data consortium

    (1995)
  • L.F. Barrett et al.

    The amygdala and the experience of affect

    Social Cognitive and Affective Neuroscience

    (2007)
  • L.F. Barrett et al.

    The embodiment of emotion

  • L.F. Barrett et al.

    The experience of emotion

    Annual Review of Psychology

    (2007)
  • K. Blair et al.

    Neural response to self- and other referential praise and criticism in generalized social phobia

    Archives of General Psychiatry

    (2008)
  • G.H. Bower

    Mood and memory

    American Psychologist

    (1981)
  • A.E. Cavanna et al.

    The precuneus: A review of its functional anatomy and behavioural correlates

    Brain

    (2006)
  • A.D. Craig

    How do you feel? Interoception: The sense of the physiological condition of the body

    Nature Reviews Neuroscience

    (2002)
  • A.D. Craig

    Interoception and emotion: A neuroanatomical perspective

  • A.D. Craig

    How do you feel-now? The anterior insula and human awareness

    Nature Reviews Neuroscience

    (2009)
  • F.I.M. Craik et al.

    In search of the self: A positron emission tomography study

    Psychological Science

    (1999)
  • C. Cristinzio et al.

    Integration of gaze direction and facial expression in patients with unilateral amygdala damage

    Brain

    (2011)
  • H.D. Critchley

    Neural mechanisms of autonomic, affective, and cognitive integration

    Journal of Comparative Neurology

    (2005)
  • H.D. Critchley et al.

    Neural systems supporting interoceptive awareness

    Nature Neuroscience

    (2004)
  • Cited by (57)

    • Anticipatory feelings: Neural correlates and linguistic markers

      2020, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      In particular, “transforming” subjective feelings into words may not only induce emotions and feeling states, but may also modulate emotion perception (Barrett et al., 2016; Herbert et al., 2013; Lindquist et al., 2015). Interestingly, reading words that refer to the reader’s own emotions has been found to elicit changes in neural activity in the left and right insula, amygdala, and parts of the ventral medial prefrontal cortex (Herbert et al., 2011), all known to be critically involved in the awareness of body states (interoception), in self-referential processing of emotions and in feelings of emotional ownership (Northoff et al., 2006). The meta-analysis conducted within this review (see section 5) supports an overlap of activation in dedicated brain regions for language and affective feelings including the insula.

    • Shared Mechanisms May Support Mnemonic Benefits from Self-Referencing and Emotion

      2018, Trends in Cognitive Sciences
      Citation Excerpt :

      We propose here that emotional or self-referential information engages overlapping processes that are beneficial to memory encoding (see Glossary), increasing the likelihood that information is retained in memory. Many before us have written about the overlap between the experience of emotion and self-relevance (e.g., [8–11]). It is hard to envisage real-world scenarios in which emotion is elicited but the event contains no self-importance, and some theories of emotion dictate that self-relevance must be present for emotion to arise (e.g., [12]).

    View all citing articles on Scopus

    The complete list of the words used in this study (original and translation) is available from the authors upon request.

    View full text