ReviewRelevance to self: A brief review and framework of neural systems underlying appraisal
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.
References (107)
Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices
Brain Research Bulletin
(2000)- et al.
The neural correlates of maternal and romantic love
Neuroimage
(2004) - et al.
A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events
Neuroimage
(2001) - et al.
Cognitive and emotional influences in anterior cingulate cortex
Trends in Cognitive Sciences
(2000) - et al.
Parallel networks operating across attentional deployment and motion processing: a multi-seed partial least squares fMRI study
Neuroimage
(2006) Forebrain emotional asymmetry: a neuroanatomical basis?
Trends in Cognitive Sciences
(2005)- et al.
Self-referential reflective activity and its relationship with rest: a PET study
Neuroimage
(2005) - et al.
The functional neuroanatomy of emotion and affective style
Trends in Cognitive Sciences
(1999) - et al.
Visual areas in the temporal cortex of the macaque
Brain Research
(1979) Cerebellar contributions to cognition
Neuron
(1996)
The neural bases of cognitive conflict and control in moral judgment
Neuron
Brain correlates of aesthetic judgment of beauty
Neuroimage
Reflective self-awareness and conscious states: PET evidence for a common midline parietofrontal core
Neuroimage
A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI
Neuroimage
Fear and anxiety: animal models and human cognitive psychophysiology
Journal of Affective Disorders
The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain
Trends in Neuroscience
A post-processing/region of interest (ROI) method for discriminating patterns of activity in statistical maps of fMRI data
Journal of Neuroscience Methods
A review of systems and networks of the limbic forebrain/limbic midbrain
Progress in Neurobiology
Dissociable amygdala and orbitofrontal responses during reversal fear conditioning
Neuroimage
Mining the posterior cingulate: segregation between memory and pain components
Neuroimage
Functional neuroanatomy of aversion and its anticipation
Neuroimage
Cortical midline structures and the self
Trends in Cognitive Sciences
Self-referential processing in our brain—a meta-analysis of imaging studies on the self
Neuroimage
The neural correlates of direct and reflected self-knowledge
Neuroimage
Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation
Neuroimage
Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI
Neuroimage
Activation of the medial prefrontal cortex and extended amygdala by individual ratings of emotional arousal: a fMRI study
Biological Psychiatry
Neural correlates of individual ratings of emotional salience: a trial-related fMRI study
Neuroimage
Extinction learning in humans: role of the amygdala and vmPFC
Neuron
Neurobiology of emotion perception I: The neural basis of normal emotion perception
Biological Psychiatry
Neurobiology of emotion perception II: Implications for major psychiatric disorders
Biological Psychiatry
Prediction error for free monetary reward in the human prefrontal cortex
Neuroimage
Neural correlates of “hot” and “cold” emotional processing: a multilevel approach to the functional anatomy of emotion
Neuroimage
Self-appraisal decisions evoke dissociated dorsal–ventral aMPFC networks
Neuroimage
Metacognitive evaluation, self-relevance, and the right prefrontal cortex
Neuroimage
Cortical Activations during judgments about the self and an other person
Neuropsychologia
The functional neuroanatomy of autobiographical memory: a meta-analysis
Neuropsychologia
Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain
Neuroimage
Cytology and functionally correlated circuits of human posterior cingulate areas
Neuroimage
Parietal lobe contributions to episodic memory retrieval
Trends in Cognitive Sciences
Attentional activation of the cerebellum independent of motor involvement
Science
Meeting of minds: the medial frontal cortex and social cognition
Nature Reviews Neuroscience
Lesions of the human amygdala impair enhanced perception of emotionally salient events
Nature
Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey
Journal of Comparative Neurology
Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey
Journal of Comparative Neurology
Cerebellar outflow lesions: a comparison of movement deficits resulting from lesions at the levels of the cerebellum and thalamus
Annals of Neurology
Deciding advantageously before knowing the advantageous strategy
Science
Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making
Journal of Neuroscience
Role of the amygdala in decision-making
Annals of New York Academy of Science
Painful stimuli evoke different stimulus–response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study
Brain
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