Elsevier

NeuroImage

Volume 31, Issue 1, 15 May 2006, Pages 440-457
NeuroImage

Self-referential processing in our brain—A meta-analysis of imaging studies on the self

https://doi.org/10.1016/j.neuroimage.2005.12.002Get rights and content

Abstract

The question of the self has intrigued philosophers and psychologists for a long time. More recently, distinct concepts of self have also been suggested in neuroscience. However, the exact relationship between these concepts and neural processing across different brain regions remains unclear. This article reviews neuroimaging studies comparing neural correlates during processing of stimuli related to the self with those of non-self-referential stimuli. All studies revealed activation in the medial regions of our brains' cortex during self-related stimuli. The activation in these so-called cortical midline structures (CMS) occurred across all functional domains (e.g., verbal, spatial, emotional, and facial). Cluster and factor analyses indicate functional specialization into ventral, dorsal, and posterior CMS remaining independent of domains. Taken together, our results suggest that self-referential processing is mediated by cortical midline structures. Since the CMS are densely and reciprocally connected to subcortical midline regions, we advocate an integrated cortical–subcortical midline system underlying human self. We conclude that self-referential processing in CMS constitutes the core of our self and is critical for elaborating experiential feelings of self, uniting several distinct concepts evident in current neuroscience.

Introduction

The question of the self has been one of the most salient problems throughout the history of philosophy and more recently also in psychology (Gallagher, 2000, Gallagher and Frith, 2003, Metzinger and Gallese, 2003, Northoff, 2004). For example, William James distinguished between a physical self, a mental self, and a spiritual self. These distinctions seem to reappear in recent concepts of self as discussed in neuroscience (Panksepp, 1998a, Panksepp, 1998b, Panksepp, 2003, Panksepp, 2005b, Damasio, 1999, Gallagher, 2000, Stuss et al., 2001, Churchland, 2002, Kelley et al., 2002, Lambie and Marcel, 2002, LeDoux, 2002, Turk et al., 2002, Damasio, 2003a, Damasio, 2003b, Gallagher and Frith, 2003, Keenan et al., 2003, Kircher and David, 2003, Turk et al., 2003, Vogeley and Fink, 2003, Dalgleish, 2004, Marcel and Lambie, 2004, Northoff and Bermpohl, 2004). Damasio (1999) and Panksepp, 1998a, Panksepp, 1998b, Panksepp, 2003 suggest a “proto-self” in the sensory and motor domains, respectively, which resembles William James's description of the physical self. Similarly, what has been described as “minimal self” (Gallagher, 2000, Gallagher and Frith, 2003) or “core or mental self” (Damasio 1999) might correspond more or less to James' concept of mental self. Finally, Damasio's (Damasio 1999) “autobiographical self” and Gallagher's (Gallagher, 2000, Gallagher and Frith, 2003) “narrative self” strongly rely on linking past, present, and future events with some resemblances to James' spiritual self.

The distinct concepts of self differ in the class of stimuli and their specific material or content reflecting what is called different domains. The “proto-self” refers to the domain of the body, whereas the “autobiographical self” reflects the domain of memory. Other concepts of self like the emotional self (Fossati et al., 2003, Fossati et al., 2004), the spatial self (Vogeley and Fink, 2003, Vogeley et al., 2004), the facial self (Keenan et al., 2000, Keenan et al., 2001, Keenan et al., 2003), the verbal or interpreting self (Turk et al., 2003), and the social self (Frith and Frith, 1999, Frith and Frith, 2003) refer to further domains.

What remains unclear, however, is what unites these distinct concepts of self allowing us to speak of a self in all cases. In this article, we assume that processing of stimuli as self-referential, self-referential processing, is common to the distinct concepts of self in the different domains. This has also been described as ‘self-related’ or ‘self-relevant’ processing (Craik and Hay, 1999, Kelley et al., 2002, Schore, 2003, Turk et al., 2003, Northoff and Bermpohl, 2004, Phan et al., 2004a, Phan et al., 2004b). Self-referential processing concerns stimuli that are experienced as strongly related to one's own person. Typical examples are the way we perceive pictures of ourselves or close friends versus pictures of completely unknown people or pictures of our houses where we spent our childhood versus pictures of any unknown house, etc. Such comparisons are possible in different sensory modalities. Without going deeply into abstract philosophical considerations, we would like to give a brief theoretical description of what we mean by the terms ‘experience’, ‘strongly related’, and ‘to one's person’. ‘Experience’ refers to phenomenal experience such as, for example, the feeling of love, the smell of a rose, or the feeling of mineness. Thus, we focus on the subjective aspect of experience that is described as the “phenomenal aspect” (Block, 1996, Chalmers, 1996). The subjective aspect of experience as prereflective is often distinguished from its reflective or cognitive aspects (see also Fig. 5). The latter refer to veridical information processing and objective reasoning. Being in love from that point of view refers to psychological questions concerning motivation and causes for the emotional state (Block, 1996, Chalmers, 1996). Our definition of self-referential processing by experience implies a focus on the implicit, subjective, and phenomenal aspects (to feel or experience self-referential stimuli) what Kircher and David (2003) call “self-qualia” and Zahavi (2003) describe as “prereflective” (Legrand 2003, Gallagher and Zahavi, 2005, Legrand, 2005), whereas our focus is less on associated cognitive and reflective functions (see also Fig. 5) allowing to make it explicit (to know about or to be aware of stimuli as self-referential). As such, we distinguish self-referential processing also from what is commonly called “insight” which we consider to presuppose cognitive and reflective functions rather than simply pure subjective and phenomenal aspects (Kircher and David, 2003).

The term ‘strongly related’ points out the process of associating and linking intero- and exteroceptive stimuli with a particular person. The main feature here is not the distinction between diverse sensory modalities but rather the linkage of the different stimuli to the individual person, i.e., to its self. What unifies and categorizes stimuli in this regard is no longer their sensory origin but the strength of their relation to the self (this is what Kircher and David (2003) call ‘ipseity’). The more the respective stimulus is associated with the person's sense of belongingness, the more strongly it can be related to the self. We assume that the strength of the self-stimulus relation cannot be determined in absolute terms but only relatively since it depends on the respective context (which includes autobiographical, social, spatial, and various other factors). The process of relating stimuli to the self can thus not be considered an isolated process but rather an embedded process that depends on the respective environmental context (Clark, 1999, Northoff, 2004). The self-stimulus relation results in what has been called “mineness”. Lambie and Marcel (2002) speak of an “addition of the ‘for me’” by means of which that particular stimulus becomes “mine” resulting in “mineness” (Metzinger, 2003).

The self is usually characterized by a more intense emotional subjectivity which points out that stimuli are considered in more value-laden ways. When objects and events are viewed through the ‘eyes’ of the self, stimuli are no longer simply objective aspects of the world, but they typically become emotionally colored, and thereby more intimately, related to one's sense of self. Another feature of the self is that it is characterized in relation to both physical and psychological stimuli. Physical stimuli include those from one's own body such as face, arms, interoceptive bodily functions, etc., whereas psychological stimuli encompass propositional knowledge about one's self including episodic memories as well as more subtle evaluations such as perspectives on one's body image, worthiness, etc. (Gillihan and Farah, 2005). Psychological self-referential stimuli were, for example, investigated by Kelley et al. (2002) in a trait adjective judgment task. In that study, participants were asked to judge trait adjectives (for example, ‘polite’) as to whether they properly described the participants themselves (self-referential), the current U.S. President (other-referential), or a given case (case-referential). Self-referential processing might not only concern verbal stimuli but also those from other psychological or physical domains like for example autobiographical, emotional, motor, and facial stimuli.

Finally, we do not necessarily wish to imply that the reflective self constitutes a substantial material entity; there may even be no fixed entity behind the continuously ongoing self-referential processing what James called the “stream of thought” (James, 1892). Instead, here, we characterize the self by an individual's relation to stimuli in the world and thus by self-referential stimuli. The reflective self is not considered as a fixed and isolated entity but as a context-dependent and thus embedded process. This process is manifest in subjective experience—the self we consider here is an experiential self that mediates ownership of experience (Zahavi, 2003, Gallagher and Zahavi, 2005, Legrand, 2005). Our presupposition in this paper is that self-referential processing constitutes the “experiential self” which can be considered to be a way that one reflects on ones experiences in a very fundamental way. Below, this processing there may be a more fundamental core self that is more strictly a prereflective and rather affective representation of internal and external stimuli including their subjective (or phenomenal) experience as such that is essential for any reflective awareness to become possible (Panksepp, 1998a, Panksepp, 1998b, Damasio, 1999).

Recently, the question of self has also become a topic in neuroimaging. Though current studies remain unable to account for all the distinct and subtle aspects of self-referential processing discussed above, they at least are able to reveal various regions in association with self-related tasks (see also Legrand, 2005) for advancing a similar argument about the discrepancy between empirical designs and conceptual distinctions). In addition to various regions in our brains' medial cortex (see below for details), a variety of other regions like ventro- and dorsolateral prefrontal cortex, lateral parietal cortex, bilateral temporal poles, insula, and subcortical regions, including brain stem, colliculi, periaqueductal gray (PAG), and hypothalamus/hypophysis, have been observed to be activated during self-related tasks (LeDoux, 1996, Gazzaniga, 1998, Panksepp, 1998a, Panksepp, 1998b, Panksepp, 2003, Panksepp, 2005b, Damasio, 1999, Damasio, 2003a, Damasio, 2003b, Gallagher, 2000, Rolls, 2000a, Rolls, 2000b, LeDoux, 2002, Gallagher and Frith, 2003, Keenan et al., 2003, Kircher and David, 2003, Vogeley and Fink, 2003, Gillihan and Farah, 2005). This regional heterogeneity raises the question of so-called core regions being commonly involved in the different self-related tasks. In addition to lateral cortical and subcortical regions, several neuroimaging studies report involvement of various medial cortical regions. These include the medial orbital prefrontal cortex (MOFC), the ventromedial prefrontal cortex (VMPFC), the sub/pre- and supragenual anterior cingulate cortex (PACC, SACC), the dorsomedial prefrontal cortex (DMPFC), the medial parietal cortex (MPC), the posterior cingulate cortex (PCC), and the retrosplenial cortex (RSC) (see also Fig. 5 in Gillihan and Farah, 2005). Recently, these regions have been subsumed under the term cortical midline structures (CMS) (see Fig. 1) and characterized as an anatomical and functional unit (Northoff and Bermpohl, 2004). What remains unclear, however, is whether activation in CMS is related to self-referential processing per se or to some task-specific processes reflecting the respective sensory–perceptual processing domains (Gillihan and Farah, 2005). If the CMS are associated with self-referential processing per se, activation in these regions should be observed in self-related tasks across all domains and sensory modalities, remaining task-independent. In the converse case, activation in CMS should occur only in self-related tasks in specific cognitive domains (or even sensory modalities) but not in other domains (or sensory modalities), showing task dependence or specificity.

The aim of the present article is to investigate whether there are core medial cortical regions that are commonly involved in self-related tasks across different cognitive domains and sensory modalities. For that purpose, we review neuroimaging studies with self-related tasks in different domains employing different stimuli such as trait adjectives, memories, emotions, and movements. We assume that there may be common regions in all such studies and that these core regions might predominantly be situated in cortical midline structures. Based on our hypothesis, we focus on reported involvement of medial cortical region in a series of relevant imaging studies. In addition, we test for functional specialization within the CMS using cluster and factor analysis. We assume that functional specialization within the CMS is not oriented on specific cognitive or perceptual domains but rather on some other principles like for example how meaningful a stimulus is to an individual. We will also shed some light on anatomical and functional linkage of CMS to subcortical midline regions and the role of both systems in constituting the multitudes of selves that have been proposed in the literature. This is complemented by discussing the linkage of self-referential processing in CMS to higher-order processing in lateral prefrontal cortical regions. Finally, we briefly discuss our results and their implications within the context of neurophilosophical conceptions of the self.

Section snippets

Study selection

We analyzed 27 PET and fMRI studies on self-related tasks published between 2000 and 2004 (see Table 1). We used a rather broad and unspecific definition of self-related tasks describing all tasks where some material or content had to be related to the persons themselves, i.e., their own selves. Studies included only those with healthy subjects, whereas those on neurological or psychiatric disorders were excluded. The following inclusion criteria were applied:

  • 1.

    Only studies measuring neural

Self-referential processing in the verbal domain

Several studies have investigated verbal tasks in relation to the self. For example, Kelley et al. (2002) investigated a trait adjective judgment task comparing self-, other-, and case-referential adjectives (see Introduction for more complete description). They demonstrated that the VMPFC and the DMPFC were selectively engaged in the self-related condition. Employing auditorily delivered statements, Johnson et al. (2002) compared judgments about one's own abilities, traits, and attitudes (such

Sensory processing and self-referential processing

Our review of neuroimaging studies reveals a set of commonly activated regions, within the extended CMS, during self-related tasks using a diverse set of sensory modalities. Activation in CMS must therefore be considered independent of the sensory mode within which the self-related stimuli were presented. Such sensory independence of neural activity in CMS can be observed in all domains. This is paradigmatically reflected in the emotional domain. Regardless of whether emotions were induced

Conclusion

We assume self-referential processing to be at the core of what is called the self. Self-referential processing accounts for distinguishing stimuli related to one's own self from those that are not relevant to one's own concerns. As such, self-referential processing might be at the bottom of what has been called “mental or core self” (Damasio, 1999), “experiential self” (Lambie and Marcel, 2002, Zahavi, 2003), “prereflective self” (Gallagher and Zahavi, 2005, Legrand, 2005), or “minimal self” (

Acknowledgments

The work was made possible by grants from the German Exchange Service (Postdoc-Programme) to F.B. (DAAD, D/02/46858), the German Research Foundation (DFG, 304/1-4) to G.N., and the Salus Stiftung to G.N.

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