Brain imaging of the self – Conceptual, anatomical and methodological issues☆
Introduction
The problem of the self has been investigated extensively in neuroscience using most notably brain imaging (Gillihan and Farah, 2005, Legrand and Ruby, 2009, Metzinger and Gallese, 2003, Northoff and Bermpohl, 2004, Northoff et al., 2006). Comparing self- vs. non-self-specific stimuli, brain imaging studies observed neural activity changes in various medial cortical regions including the perigenual anterior cingulate cortex (pACC), dorsomedial prefrontal cortex (MPFC) and the posterior cingulate cortex (PCC) (Kelley et al., 2002, Mitchell et al., 2005, Northoff and Bermpohl, 2004, Northoff et al., 2006, Platek et al., 2006, Uddin et al., 2007, Yaoi et al., 2009, Zhu et al., 2007). The results obtained in single studies were however contradicted by recent meta-analyses on imaging studies of the self (Gillihan and Farah, 2005, Legrand and Ruby, 2009) which do not support the specific association of medial cortical regions, i.e., the cortical midline structures (CMS) (Northoff & Bermpohl, 2004) with self-specific stimuli. Instead, they demonstrated that theses regions may also be implicated in processing non-self-specific stimuli as, for instance personal familiar stimuli (Gillihan and Farah, 2005, Seger et al., 2004) or task-specific requirements like general evaluation (Legrand & Ruby, 2009). However, the association of familiarity and task-specific requirements with the cortical midline structures during presentation of self- and non-self-specific stimuli remains to be investigated.
In addition to the cortical midline structures, neural processing of self-specific stimuli has recently been also associated with resting state activity in the default-mode network (DMN) (Buckner et al., 2008, Raichle et al., 2001). Since the regions of the DMN strongly overlap with those of the cortical midline structures, some authors speak even of ‘default-self’ arguing that the self may be more or less identical with the high resting state activity observed in these regions (Boly et al., 2008, Christoff et al., 2003, David et al., 2007, Golland et al., 2007, Gusnard et al., 2001, Wicker et al., 2003). If so the self may be assumed to be based purely on internal processing, i.e., the brain’s resting state activity, and thus distinguished from external processing, i.e., stimulus-induced activity. While there is some indirect support for the regional overlap in especially the pACC between resting state activity and neural activity induced by self-specific stimuli (D’Argembeau et al., 2005, Schneider et al., 2008), direct experimental demonstration is thus far lacking. This may also be due in part to the methodological difficulty of measuring resting state activity in relation to self-specific stimuli with the latter violating the former.
There may be several reasons why the data regarding the neuroanatomical basis of the self conflict. One of them may be that differing neuroscientific and philosophical concepts of the self. (Legrand and Ruby, 2009, Northoff et al., 2006) may yield different results regarding its underlying anatomy. What exactly is meant by self when we for instance compare the neural effects of judging self- and non-self-specific stimuli? There may be other concepts of self which require a different experimental design. One possibility would be to determine if the self as judged by its internal contents is already present in the resting state independent of externally presented stimuli. This is suggested by the strong overlap between cortical midline structures (CMS) and the DMN.
Another issue is that how we organize and interpret the hierarchical structure of brain anatomy with reference to the concept of anatomically “midline structures” has special relevance for our understanding of the neuroanatomy of the self Feinberg (2009, this issue) suggests that the neural hierarchy is organized along an anatomically medial–lateral or central–peripheral dimension. This results in anatomically concentric rings that extend the length of the neuroaxis from subcortical to cortical zones (Feinberg, this issue). According to this organization, the medial (interoself) system corresponds to the innermost rings and is related to self-related and homeostatic processes, the lateral (peripheral) system is anatomically related to the outer rings and subserves exterosensorimotor processes, and the middle rings represent an integrative system that mediates between the other two. Rostrally, the cortical midline regions (Northoff and Bermpohl, 2004, Northoff et al., 2006) are in part paralimbic regions that correspond to the medial- inner rings It would be of interest to see how the imaging data map onto this medial-inner and lateral outer distinction.
Third, in addition to conceptual and anatomical issues, we need to consider some methodological issues. When observing the effects of self- and non-self-specific stimuli current imaging studies treat the self as independent variable on neural activity, while the neural activity itself as measured with fMRI is considered the dependent variable. This informs us about neural activity related to the stimulus itself, e.g., the stimulus-induced activity but it may not provide any insight into the brain’s intrinsic activity, e.g., its resting state activity, and how it modulates the stimulus-induced activity, e.g., rest–stimulus interaction (Northoff, Qin, & Nakao, 2010) However as there is strong overlap between stimulus-induced activity in CMS and resting state activity in the DMN, one may need to consider the latter, e.g., the resting state activity, in experimental designs. To do that, however, we may need to modify our current methodological and experimental approaches to the self in brain imaging studies.
Section snippets
Content-based concepts of the self
The question of the self has been one of the most salient problems throughout the history of philosophy, psychology and neuroscience (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 distinct selves even may be related to distinct brain regions (Churchland, 2002, Dalgleish, 2004, Damasio, 1999, Damasio, 2003a, Damasio, 2003b, Gallagher, 2000,
Neuroanatomy: radial-concentric organization and subcortical–cortical systems in the brain
Many imaging studies on the self demonstrated involvement of cortical midline structures like the VMPFC, the PACC, the DMPFC and the PCC in the neural processing of self-specific stimuli (Northoff et al., 2006). The self-specificity of the neural activity in the CMS has been questioned on several grounds. At the same time the concept of cortical midline structures has been extended to include subcortical midline regions (Feinberg, 2009, Northoff and Panksepp, 2008, Panksepp and Northoff, 2009).
Conclusions
We here investigated two problems central in the imaging of the self, conceptual–experimental and anatomical issues. Conceptually, we distinguished between content- and process-based views of the self which were also shown to require different experimental approaches. The content-based view defines the self by specific contents (bodily, mental or autobiographical) and searches for the neural correlates of these contents and their respective stimulus-induced activity. The process-based view, in
Acknowledgments
The work on this paper was supported by grants from the CRC, the CIHR, and the CIHR-EJLB to GN.
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This article is part of a special issue of this journal on “Brain and Self: Bridging the Gap”.
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These authors have contributed equally.