PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of scanLink to Publisher's site
 
Soc Cogn Affect Neurosci. Feb 2013; 8(2): 121–122.
Published online Jan 16, 2013. doi:  10.1093/scan/nss134
PMCID: PMC3575729
The neuropsychology of disgust
Michael Koenigscorresponding author
Department of Psychiatry, University of Wisconsin-Madison, Madison, WI 53719, USA
corresponding authorCorresponding author.
Correspondence should be addressed to Michael Koenigs, Department of Psychiatry, University of Wisconsin-Madison, Madison, WI 53719, USA. E-mail: mrkoenigs/at/wisc.edu
Received November 8, 2012; Accepted November 13, 2012.
Beginning with the landmark case of Phineas Gage (Harlow, 1868), studies of neurological patients with ventromedial prefrontal cortex (vmPFC) damage have time and again demonstrated a critical role for this brain area in various aspects of emotion, social cognition and decision-making. The importance of vmPFC for social and affective function is further underscored by a host of clinical neuroimaging studies, which have demonstrated abnormal patterns of vmPFC activity in psychiatric disorders such as major depression, post-traumatic stress disorder, obsessive–compulsive disorder, schizophrenia, psychopathy and autism. Specifying the essential functions of vmPFC may therefore be a key step in elucidating the neuropathophysiological mechanisms underlying diverse forms of socio-affective dysfunction in mental illness. In this regard, lesion studies are an indispensible methodological approach; the loss of vmPFC function through focal lesions (e.g. as a result of tumor, stroke or aneurysm) affords a unique opportunity to assess in humans the causal contribution of vmPFC to particular psychological faculties. In this issue, Ciaramelli et al. (2012b) present the latest advance in this line of lesion patient research.
The investigators focus on the negative emotion ‘disgust’, which can apply to physical objects, such as rotten food or bodily excrement, as well as immoral or socially unaccepted behavior, such as lying or cheating. To determine whether vmPFC is especially critical for the social/moral connotation of disgust, the study team developed a task involving a series of disgust-inducing hypothetical scenarios, with the key experimental manipulation being the subcategory of disgust featured in each scenario. ‘Core’ disgust scenarios involved contamination or physical impurity (e.g. deciding whether to eat a slice of pizza from an ant-infested kitchen), whereas ‘interpersonal’ disgust scenarios involved contact with an unsavory or deviant other (e.g. deciding whether to share a park bench with a vagrant) and ‘moral’ disgust scenarios involved exposure to a moral transgression (e.g. deciding whether to divulge a friend’s infidelity to his wife). The investigators found a remarkably specific effect of vmPFC damage; the vmPFC lesion patients exhibited normal sensitivity to ‘core’ and ‘moral’ disgust-inducing actions but endorsed an abnormally high proportion of the ‘interpersonal’ disgust actions. These results therefore associate vmPFC damage with a relatively specific insensitivity to the social status of others, rather than a general flattening of negative affect or overall decision-making impairment. These intriguing findings illuminate several interrelated issues in contemporary social, cognitive and affective neuroscience.
One is the iterative fractionation and refinement of broad constructs, such as ‘disgust’ and ‘morality’, into subcomponents with distinct underlying neural substrates. In recent years, a number of studies have converged to suggest that the feeling of ‘moral’ disgust is derived from, or at least psychologically and physiologically related to, the feeling of ‘physical’ or ‘core’ disgust. For example, one study showed that the muscle activity that characterizes the facial expression of physical disgust (raising the upper lip and wrinkling the nose) is elicited not only by drinking unpleasant-tasting liquids and viewing pictures of contamination, but also when experiencing unfair treatment, which represents a more abstract moral transgression (Chapman et al., 2009). Another set of studies have shown that experimental manipulations of the feeling of ‘core’ disgust can influence the severity of subsequent moral judgment (Wheatley and Haidt, 2005; Schnall et al., 2008a, b). Despite these putative psychological links between ‘core’ and ‘moral’ disgust, one functional magnetic resonance imaging (fMRI) study has demonstrated partially dissociable patterns of neural activity, with notably greater mPFC activity for ‘moral’ versus ‘core’ disgust stimuli (Schaich Borg et al., 2008). This subspecification strategy has also been effectively applied to domains of moral judgment outside of disgust. For example, a pioneering fMRI study of moral judgment distinguished between ‘personal’ and ‘impersonal’ harms, and identified a number of brain areas, including mPFC, that respond differently to scenarios depicting one or the other type of harm (Greene et al., 2001). Moreover, abnormalities in judgments of personal (but not impersonal) harms have been associated with damage to vmPFC (Ciaramelli et al., 2007; Koenigs et al., 2007) as well as administration of specific psychoactive drugs, such as citalopram (Crockett et al., 2010) and lorazepam (Perkins et al., 2012). Similarly, differentiating between intentional and accidental harms has revealed distinct patterns of neural activity (Young et al., 2007), as well as selective abnormalities in moral judgment following vmPFC damage (Young et al., 2010a; Ciaramelli et al., 2012a) and transcranial magnetic stimulation applied to the temporoparietal junction (Young et al., 2010b). Ciaramelli et al.’s approach thus extends a fertile strategy of linking subclasses of socio-moral judgment to distinct neuroanatomical substrates.
A related issue highlighted by this study is the potential for developing novel neuropsychological assessment instruments to probe specific aspects of social-affective function. In the realm of clinical neuropsychology, evaluation of social-affective function typically consists of simple self-report symptom inventories (e.g. Beck Depression Inventory, State-Trait Anxiety Inventory). In this respect, assessment of social-affective function lags far behind its ‘cognitive’ counterpart, where extensive batteries of performance-based tests have long been established. For example, in the domain of memory, there are dozens of standardized performance-based tests that probe the integrity of specific competencies (verbal vs. non-verbal, short-term vs. long-term, recall vs. recognition and so on). Similar batteries of performance-based tests have been developed to probe aspects of language, perception and executive function. Why are there not analogous performance-based clinical measures of social and affective function? After all, mood and anxiety disorders are the number one leading cause of disability in developed countries (WHO, 2008). Moreover, the National Institute of Mental Health proposes that a key step in the development of more effective treatments for psychiatric disorders is to identify specific domains of social, cognitive and affective dysfunction that cut across traditional diagnostic categories, and to link these domains of psychological function to their underlying neural circuitry (Insel et al., 2010; http://www.nimh.nih.gov/research-funding/rdoc/index.shtml). A critical component of this strategy is improving the measurement of specific social and emotional competencies. The present study by Ciaramelli et al., which suggests an association between a relatively specific socio-affective impairment (sensitivity to the social status of others) and a relatively focal brain area (vmPFC), appears to be a step in this direction.
Of course, vmPFC is known to play a far more diverse role in social and affective function than simply ‘sensitivity to the social status of others.’ This study thus begs the overarching question: what exactly does vmPFC do? Most current systems-level research on vmPFC focuses on one of three neural circuits. One circuit, involving the vmPFC and amygdala, is thought to underlie the regulation of negative emotion (Phelps et al., 2004; Milad et al., 2006; Rauch et al., 2006). A second circuit, involving the vmPFC and ventral striatum, is thought to underlie aspects of reinforcement learning and subjective reward value (McClure et al., 2004; O'Doherty, 2004, 2011). A third circuit, involving the vmPFC, dorsomedial PFC, posterior cingulate cortex/precuneus and inferior lateral parietal cortex (the so-called ‘default mode network’) is thought to underlie aspects of self-referential processing and rumination (Buckner et al., 2008; Qin and Northoff, 2011; Whitfield-Gabrieli et al., 2011). Is it the case that vmPFC consists of multiple, functionally and anatomically distinct subregions that correspond to each of these circuits? For example, might a subgenual sector have a particularly important role in modulating amygdala activity, whereas a pregenual sector may have a greater role in modulating the self-processing network? Or, alternatively, might vmPFC subserve some higher order meta-function, which integrates the activity of several different circuits representing various elements of social and affective processing, and translates these into an adaptive behavioral response?
Traditionally, human lesion studies have not been well suited to address the possibility of functionally and anatomically distinct subunits within the vmPFC. The reason for this is the gross etiology of naturally occurring lesions in this area of brain, coupled with the relative rarity of such patients. vmPFC lesion studies typically involve n = 10 or fewer vmPFC lesion patients, making it difficult to parse the contribution of putative vmPFC subunits to the observed impairments. This study attempts to address this issue through a correlation analysis, showing opposite relationships between interpersonal disgust acceptance rates and lesion volumes in Brodmann Areas 10 and 11, respectively. Although this correlation analysis represents a thoughtful (if only preliminary) approach to potential functional heterogeneity within vmPFC, a more comprehensive understanding will likely depend on increasing patient sample sizes.
In sum, through an inventive combination of moral psychology and behavioral neurology approaches, Ciaramelli et al. have demonstrated a critical role for vmPFC in processing interpersonal disgust. This study exemplifies the capability of human lesion studies to yield novel insight into the neuropsychological mechanisms underlying social and affective processing.
Acknowledgments
This work was supported by a grant from the National Institute of Mental Health (MH086787).
  • Buckner RL, Andrews-Hanna JR, Schacter DL. The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci. 2008;1124:1–38. [PubMed]
  • Chapman HA, Kim DA, Susskind JM, Anderson AK. In bad taste: evidence for the oral origins of moral disgust. Science. 2009;323:1222–6. [PubMed]
  • Ciaramelli E, Braghittoni D, di Pellegrino G. It is the outcome that counts! Damage to the ventromedial prefrontal cortex disrupts the integration of outcome and belief information for moral judgment. J Int Neuropsychol Soc. 2012a;18:962–71s. [PubMed]
  • Ciaramelli E, Muccioli M, Ladavas E, di Pellegrino G. Selective deficit in personal moral judgment following damage to ventromedial prefrontal cortex. Soc Cogn Affect Neurosci. 2007;2:84–92. [PMC free article] [PubMed]
  • Ciaramelli E, Sperotto RG, Mattioli F, di Pellegrino G. Damage to the ventromedial prefrontal cortex reduces interpersonal disgust. Soc Cogn Affect Neurosci. 2012b Epub ahead of print. [PMC free article] [PubMed]
  • Crockett MJ, Clark L, Hauser MD, Robbins TW. Serotonin selectively influences moral judgment and behavior through effects on harm aversion. Proc Natl Acad Sci U S A. 2010;107:17433–38. [PubMed]
  • Greene JD, Sommerville RB, Nystrom LE, Darley JM, Cohen JD. An fMRI investigation of emotional engagement in moral judgment. Science. 2001;293:2105–8. [PubMed]
  • Harlow JM. Recovery from the passage of an iron bar through the head. Publ Massachusetts Med Soc. 1868;2:327–47.
  • Insel T, Cuthbert B, Garvey M, et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry. 2010;167:748–51. [PubMed]
  • Koenigs M, Young L, Adolphs R, et al. Damage to the prefrontal cortex increases utilitarian moral judgements. Nature. 2007;446:908–11. [PMC free article] [PubMed]
  • McClure SM, York MK, Montague PR. The neural substrates of reward processing in humans: the modern role of fMRI. The neuroscientist: a review journal bringing neurobiology. Neurol Psychiatr. 2004;10:260–8. [PubMed]
  • Milad MR, Rauch SL, Pitman RK, Quirk GJ. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol. 2006;73:61–71. [PubMed]
  • O'Doherty JP. Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr Opin Neurobiol. 2004;14:769–76. [PubMed]
  • O'Doherty JP. Contributions of the ventromedial prefrontal cortex to goal-directed action selection. Ann N Y Acad Sci. 2011;1239:118–29. [PubMed]
  • Perkins AM, Leonard AM, Weaver K, et al. A dose of ruthlessness: interpersonal moral judgment is hardened by the anti-anxiety drug lorazepam. J Exp Psychol Gen. 2012 Epub ahead of print. [PubMed]
  • Phelps EA, Delgado MR, Nearing KI, LeDoux JE. Extinction learning in humans: role of the amygdala and vmPFC. Neuron. 2004;43:897–905. [PubMed]
  • Qin P, Northoff G. How is our self related to midline regions and the default-mode network? Neuroimage. 2011;57:1221–33. [PubMed]
  • Rauch SL, Shin LM, Phelps EA. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research—past, present, and future. Biol Psychiatry. 2006;60:376–82. [PubMed]
  • Schaich Borg J, Lieberman D, Kiehl KA. Infection, incest, and iniquity: investigating the neural correlates of disgust and morality. J Cogn Neurosci. 2008;20:1529–46. [PMC free article] [PubMed]
  • Schnall S, Benton J, Harvey S. With a clean conscience: cleanliness reduces the severity of moral judgments. Psychol Sci. 2008a;19:1219–22. [PubMed]
  • Schnall S, Haidt J, Clore GL, Jordan AH. Disgust as embodied moral judgment. Pers Soc Psychol Bull. 2008b;34:1096–109. [PMC free article] [PubMed]
  • Wheatley T, Haidt J. Hypnotic disgust makes moral judgments more severe. Psychol Sci. 2005;16:780–4. [PubMed]
  • Whitfield-Gabrieli S, Moran JM, Nieto-Castanon A, Triantafyllou C, Saxe R, Gabrieli JD. Associations and dissociations between default and self-reference networks in the human brain. Neuroimage. 2011;55:225–32. [PubMed]
  • WHO. The Global Burden of Disease: 2004 Update. Geneva, Switzerland: World Health Organization; 2008.
  • Young L, Bechara A, Tranel D, Damasio H, Hauser M, Damasio A. Damage to ventromedial prefrontal cortex impairs judgment of harmful intent. Neuron. 2010a;65:845–51. [PMC free article] [PubMed]
  • Young L, Camprodon JA, Hauser M, Pascual-Leone A, Saxe R. Disruption of the right temporoparietal junction with transcranial magnetic stimulation reduces the role of beliefs in moral judgments. Proc Natl Acad Sci U S A. 2010b;107:6753–8. [PubMed]
  • Young L, Cushman F, Hauser M, Saxe R. The neural basis of the interaction between theory of mind and moral judgment. Proc Natl Acad Sci U S A. 2007;104:8235–40. [PubMed]
Articles from Social Cognitive and Affective Neuroscience are provided here courtesy of
Oxford University Press