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

https://doi.org/10.1016/j.neubiorev.2006.12.003Get rights and content

Abstract

We argue that many similar findings observed in cognitive, affective, and social neuroimaging research may compose larger processes central to generating self-relevance. In support of this, recent findings from these research domains were reviewed to identify common systemic activation patterns. Superimposition of these patterns revealed evidence for large-scale supramodal processes, which are argued to mediate appraisal of self-relevant content irrespective of specific stimulus types (e.g. words, pictures) and task domains (e.g. induction of reward, fear, pain, etc.). Furthermore, we distinguish between two top-down sub-systems involved in appraisal of self-relevance, one that orients pre-attentive biasing information (e.g. anticipatory or mnemonic) to salient or explicitly self-relevant phenomena, and another that engages introspective processes (e.g. self-reflection, evaluation, recollection) either in conjunction with or independent of the former system. Based on aggregate patterns of activation derived from the reviewed studies, processes in a ventral medial prefrontal cortex (MPFC)–subcortical network appear to track with the former pathway, and processes in a dorsal MPFC–cortical–subcortical network with the latter. As a whole, the purpose of this framework is to re-conceive the functionality of these systems in terms of supramodal processes that more directly reflect the influences of relevance to the self.

Introduction

What is and what is not self-relevant may vary widely from one human to another, yet several lines of recent neuroimaging research implicate the presence of dedicated brain systems central to appraising the self-relevant content of one's environment and one's conscious mental events. These systems are attuned to the detection of salient environmental phenomena that convey significance to an organism (e.g. unexpected movement), yet perhaps solely in humans, these systems are able to instantiate elaborate self-relevant information from past experience to create abstract associations with stimuli, or, to instantiate such information independent of external stimuli altogether. In this way, we consider salience simply as a bottom-up propagation of sensory information sufficient for allocation of attention, whereas self-relevance is defined as top-down and generated by two integrative sub-systems, one that orients pre-attentive biasing information (e.g. anticipatory or mnemonic) to salient or explicitly self-relevant phenomena, and another that engages introspective processes (e.g. self-reflection, evaluation, recollection) either in conjunction with or independent of the former pathway. Our objective in this review is to identify convergent neuroimaging evidence for these top-down sub-systems and put forth an integrative model of the neural substrata underlying appraisal of self-relevance (ASR).

We argue that many similar findings observed in affective, cognitive, and social neuroimaging (ACS) research may compose a larger overlapping pattern indicative of central brain systems attuned to ASR. First, the component processes mediated by these systems are conceptualized as functioning at a supramodal level (Northoff and Bermpohl, 2004; Northoff et al., 2006), where supramodal is defined generally as a class of neural processes that respond to information independent of sensory modality, and as demonstrated in many neuroimaging studies, independent of stimulus type (e.g. words, pictures) and perhaps most importantly of task domain (e.g. induction of reward or fear appraisal). Second, the collective supramodal processes outlined in this review appear primarily sensitive, or specialized, to generating self-relevance. Based on recent evidence from diverse ACS paradigms requiring appraisal of self-relevant information, these processes appear localized to brain regions within the overall system. The anterior medial prefrontal cortex (MPFC) in particular is responsive to self-relevant information, though similar response patterns have also recently been characterized across extensive cortical (posterior/anterior cingulate) and subcortical systems. Contrary to the frequent observation that brain regions within these systems appear selective to information of a relatively narrow range (e.g. a ventral MPFC (vMPFC)–amygdalar ‘fear circuit’ (Lang et al., 2000), the growing presence of highly overlapping MPFC–cortical–subcortical findings across seemingly disparate ACS research instead points to the supramodal processing capacity and primacy of ASR inherent to the functions of these regions.

The component processes underlying ASR evoke large-scale neural signatures that are difficult to differentiate by specific functional contribution, though recent reviews have endeavored to do so (Amodio and Frith, 2006; Northoff and Bermpohl, 2004; Northoff et al., 2006; Ochsner et al., 2005; Phillips et al., 2003a, Phillips et al., 2003b). This difficulty may arise from the two discrete yet rapidly integrative sources of input that continuously inform ASR: extero/interoceptive information (e.g. sensory, somatic, autonomic) and introspective information (e.g. thoughts, memories). However, collective findings from recent neuroimaging research, including our own, have begun to decompose these input streams in two ways.

First, the observation that many different task domains evoke common neural response patterns suggests that the underlying supramodal systems are sensitive to self-relevant features shared by these domains. What are these features? In ACS research, task domains that convey self-relevance fall into broad cognitive–affective categories inclusive of reward (e.g. financial gain), fear (e.g. conditioned response), pain (e.g. shock), as well as affective cues spanning the emotion spectrum (e.g. using faces, scenes, words). Taken together, these task domains are inherently self-relevant to humans, as by design they require feature-based appraisal of stimuli that are predisposed to bias an internal state of a particular emotional valence (e.g. reward, fear) or arousal level. In doing so, these paradigms orient the participant (e.g. through successive presentations of an aversive picture or anticipation of a painful stimulus) to a specific biasing feature of the stimulus, where collectively these features are considered self-relevant (see Table 1 for examples of tasks requiring feature-based appraisal). Studies examining these task domains consistently identify overlapping cortical–subcortical systems inclusive of the vMPFC and anterior cingulate (ACC), dorsal–ventral striatum (Nacc), amygdala (Amg), and insula (Davidson and Irwin, 1999; Phillips et al., 2003a). In the context of these task domains, the top-down functioning of these limbic and cortical structures appears to be supramodal and responsive to target self-relevant features; but more generally, these structures are sensitive to the biased informational cues that convey implications for one's own survival, well-being, and goal potentials (e.g. to reproduce).

Second, emergent branches of ACS research are starting to converge on a distinct ASR system with experiments using self-relevant tasks that impose an explicitly self-referential contingency, where participants appraise how the stimulus makes them feel, or, whether the stimulus relates to some internal mental content (see Table 1 for specific examples of task instructions). Despite using comparable stimuli, the contextual shift to one's self as the referent of appraisal consistently evokes distinct neural structures inclusive of the ventral and dorsal MPFC (dMPFC), dorsorostral ACC, and posterior cingulate (PCC). Observations of this neural response pattern to such self-referential ‘modes’ have increased in close proportion with the burgeoning studies that compose this research domain. As such, these cortical midline structures (Northoff and Bermpohl, 2004) appear to mediate introspective processes associated with task-induced ASR. We argue that these structures constitute a distinct albeit highly integrated component of this supramodal system, the collective functioning of which enables continuous access to one's mental content (e.g. thoughts, memories). Recent neuroimaging research examining stimulus-independent self-referential processing, as well as the so-called resting state, has provided additional compelling support for this distinction. Therefore, in characterizing the integrative supramodal systems underlying ASR, we suggest two potentially separable sub-systems that together enable representation of sensory (e.g. exteroceptive and interoceptive) and introspective mental phenomena.

Section snippets

Ventral MPFC–ACC–subcortical system

Across a diverse array of ACS neuroimaging task domains, those requiring appraisal of biased (e.g. affective or arousing) stimulus features that convey general implications for survival or well being consistently identify activation in the vMPFC and ACC, Amg, striatum (ventral and dorsal), and insula. Specifically, process overlap in this sub-system is evident: in studies of reward, where the vMPFC–insula–caudate–Nacc network has been shown to differentially respond to anticipation versus

Further neuroanatomical considerations

Taken separately, the supramodal integration of subcortical and cortical systems supporting ASR follow from what is known of underlying axonal connectivity between MPFC and distal brain regions in primates and humans. Tracing studies of macaques indicate that the orbital and ventral MPFC receive robust input from inferior temporal cortices, which convey memory-enriched visual information about the global environment (Barbas, 2000; Desimone and Gross, 1979). Additionally, the orbital MPFC

Implications and conclusions

Given the present conception of two supramodal sub-systems, consisting of a vMPFC–ACC–subcortical system that orients pre-attentive biasing information (e.g. anticipatory or mnemonic) to salient or explicitly self-relevant phenomena and a dMPFC–cortical–subcortical system that mediates self-referential introspection (e.g. self-reflection, evaluation, recollection) of such phenomena, a necessary and unresolved question remains as to how these processes integrate to enable goal-directed behaviors

Acknowledgments

This work was supported in part by grants from the National Institutes of Health R01 AG021155 and R01 MH65723 and a grant from the Department of Veterans Affairs to SCJ.

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