SCIENTIF IC COMMENTARY The neurology of disgust

Emotions form part of the fabric of our minds, and the scientific attempts to map these dimensions onto the underlying neural substrates date back to the first half of the last century. It has long been suggested that emotional functions are associated with subcortical structures (e.g. Cannon, 1927; Klüver & Bucy, 1937; Hess, 1954). James Papez (1937) was the first to postulate that emotional processing is based on an interconnected cortical-subcortical system, for which later the term ‘Papez circuit’ was coined. The idea of a ‘limbic system’, defined as a functional entity responsible for all emotional experience and emotional expressions, was subsequently put forward by Paul MacLean in the early 1950s. Neuroanatomically, the ‘limbic system’ was associated with neural structures surrounding the midbrain (MacLean, 1993). A different view on the neuroanatomy of emotions emerged during the 1970s, emphasizing the role of the right hemisphere in emotion processing (Schwartz et al., 1975). However, neither of these conceptual frameworks, dominating the clinical neurosciences well into the mid-1990s, allow for selective impairments of specific emotions. In 1994, Adolphs and colleagues reported an intriguing finding, which changed the way we have to think about how emotions are organized within the brain (Adolphs et al., 1994). They investigated a person suffering from Urbach–Wiethe disease, a rare hereditary disorder which causes bilateral calcifications of the medial temporal lobes, affecting particularly the amygdala. In this person, a selective deficit in recognizing fearful faces was found, while recognition of other basic emotions such as happiness, surprise, sadness, disgust and anger was preserved. The prominent role of the amygdala in processing fear related information was later substantiated in a number of follow up studies looking at people with lesions or functional deficits of the amygdala, as well as functional imaging studies (see Calder et al., 2001 for a review). Although Huntington’s disease is commonly seen as a basal ganglia disorder, widespread atrophy of cortical and subcortical regions is common and—as noted by Lange (1981)—there is also a considerable neuronal loss within the amygdala. The latter notion motivated Sprengelmeyer and colleagues (Sprengelmeyer et al., 1996) to study whether recognition of facial expressions depicting fear is particularly impaired in Huntington’s disease. Results revealed an overall reduced ability to recognize facial expressions of emotions and, in accordance with assumptions, a pronounced deficit in fear recognition. However, very much unexpected was the disproportionate deficit in recognizing disgust, which was significantly larger than the deficit observed for recognition of fear. Nearly half of all participants tested never used the emotion label disgust to describe any of the presented facial expressions. A follow-up study of two single cases further showed that rather selective deficits in recognizing fear and disgust and even disgust alone are possible in Huntington’s disease (Sprengelmeyer et al., 1997). These reports sparked a number of subsequent studies investigating emotion processing in Huntington’s disease and other basal ganglia disorders (e.g. Suzuki et al., 2006 for Parkinson’s disease; Corcoran et al., 2007 for obsessive compulsive disorder), as well as studies looking for the neural substrate of disgust processing. Wang and colleagues reported a disproportionate impairment in disgust recognition in Chinese people suffering from Huntington’s disease (Wang et al., 2003), a finding very similar to that reported by Sprengelmeyer and colleagues in 1996. Montagne and colleagues investigated facial expression recognition in early symptomatic Huntington’s disease and found a specific impairment in recognizing anger and disgust (Montagne et al., 2006). Other studies suggest that not only the recognition of facial signals depicting disgust can be impaired in the more advanced stages of Huntington’s disease, but also the experience of this emotion. Unpleasant odours were rated as significantly less disgusting by people with Huntington’s disease than by control participants in a study by Mitchell and colleagues (Mitchell et al., 2005) and Hayes and colleagues (Hayes et al., 2007). The latter also showed that recognition of vocal stimuli depicting disgust as well as lexical and semantic aspects of disgust processing can be affected in Huntington’s disease. However, results are not always unequivocal. For example, the attempt of Milders and colleagues to show a selective or disproportionate disgust recognition deficit in Huntington’s disease failed. Instead, they reported an overall impairment in facial expression recognition, with fear and not disgust as the most affected emotion (Milders et al., 2003). They also included Huntington’s disease gene carriers in the pre-clinical stages of the disorder for which they could not show a deficit in facial expression recognition at all. doi:10.1093/brain/awm127 Brain (2007), 130, 1715^1717