Skip to main content

Disgust in Neurological Disorders

  • Chapter
  • First Online:
The Handbook of Disgust Research

Abstract

Recognition of disgust-related stimuli, disgust-related emotional responses and disgust-related emotional experiences are affected in many neurological disorders. Here, we propose a model of the putative “disgust system” in the brain, that maps recognition, responses and experience onto specific neural systems—the superior temporal cortex, the striatum (and basal ganglia) and the insular cortex. That basic mapping is used to explain the disgust-related changes in a range of neurological disorders. Recognition of facial expressions of disgust is affected in temporal lobe epilepsy, amyotrophic lateral sclerosis, Parkinson’s disease, frontotemporal dementia, and Huntington’s disease. From the point of view of the tripartite model discussed above, deficits in the recognition of disgust may not be too unexpected in these disorders. There is evidence for insular dysfunction in medial temporal lobe epilepsy, amyotrophic lateral sclerosis, behavioural variant frontotemporal dementia, Parkinson’s disease, and Huntington’s disease. All five disorders also show evidence of dysfunction of the superior temporal sulcus. Deficits in the processing of disgust-related prosody have also been found in Parkinson’s disease, medial temporal lobe epilepsy, amyotrophic lateral sclerosis, and Huntington’s disease, which again probably relate to anatomical changes in the superior temporal cortex. A loss of the capacity to demonstrate disgust-related facial expressions has been reported in Parkinson’s disease and frontotemporal dementia, as has reduced physiological responses to disgust-inducing film clips in Alzheimer’s disease, probably all secondary to changes at the level of the striatum. In contrast, the emotional experience of disgust is largely unaffected in many neurological disorders, with the exception of dementia with Lewy bodies and behavioural variant frontotemporal dementia, which have both been associated with a reduction in disgust-related experiences, possibly reflecting damage to the insular cortex. When disgust is directed at the self (self-disgust), experienced levels are actually higher (vs. healthy controls) both at baseline and in response to self-disgust inducing manipulations in Parkinson’s disease. Although disgust-related changes are largely untouched by current pharmacotherapies aimed at the core features of many neurological disorders, identifying the neural substrate for those changes is an important first step in the development of treatments targeting those changes—changes that can have a severe negative impact on the quality of life for many neurological patients.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Adolphs, R., Tranel, D., & Damasio, A. R. (2003). Dissociable neural systems for recognizing emotions. Brain and Cognition, 52, 61-9.

    Article  PubMed  Google Scholar 

  • Agosta, F., Valsasina, P., Riva, N., Copetti, M., Messina, M. J., Prelle, A., Comi, G., & Filippi, M. (2012). The Cortical Signature of Amyotrophic Lateral Sclerosis. PLoS One, 7, e42816.

    Article  PubMed  PubMed Central  Google Scholar 

  • Aho-Özhan, H. E., Keller, J., Heimrath, J., Uttner, I., Kassubek, J., Birbaumer, N., Ludolph, A. C., & Lulé, D. (2016). Perception of emotional facial expressions in amyotrophic lateral sclerosis (als) at behavioural and brain metabolic level. PLoS One, 11, e0164655.

    Article  PubMed  PubMed Central  Google Scholar 

  • Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357-81.

    Article  PubMed  Google Scholar 

  • Bathgate, D, Snowden, J S., Varma, A., Blackshaw, A., & Neary, D. (2001). Behaviour in frontotemporal dementia, Alzheimer’s disease and vascular dementia. Acta Neurologica Scandinavica, 103, 367-78.

    Article  PubMed  Google Scholar 

  • Bediou, B., Ryff, I., Mercier, B., Milliery, M., Hénaff, M-A., D’Amato, T, Bonnefoy, M., Vighetto, A., & Krolak-Salmon, P. (2009). Impaired social cognition in mild Alzheimer disease. Journal of Geriatric Psychiatry and Neurology, 22, 130–140.

    Article  PubMed  Google Scholar 

  • Blanc, F., Colloby, S. J., Philippi, N., de Pétigny, X., Jung, B., Demuynck, C., Phillipps, C., Anthony, P., Thomas, A., Bing, F., Lamy, J., Martin-Hunyadi, C., O’Brien, J. T., Cretin, B., McKeith, I., Armspach, J.-P., & Taylor, J.-P. (2015). Cortical thickness in dementia with lewy bodies and alzheimer’s disease: A comparison of prodromal and dementia stages. PLoS One, 10, e0127396.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bonora, A.., Benuzzi, F., Monti, G., Mirandola, L., Pugnaghi, M., Nichelli, P., & Meletti, S. (2011). Recognition of emotions from faces and voices in medial temporal lobe epilepsy. Epilepsy & Behavior, 20, 648–654.

    Article  Google Scholar 

  • Broicher, S. D., Kuchukhidze, G., Grunwald, T, Krämer, G., Kurthen, M., & Jokeit, H. (2012). “Tell me how do I feel”—emotion recognition and theory of mind in symptomatic mesial temporal lobe epilepsy. Neuropsychologia, 50, 118-28.

    Article  PubMed  Google Scholar 

  • Bujarski, K. A., Flashman, L., Li Z., Tosteson, T. D., Jobst, B. C., Thadani, V. M., Kobylarz, E. J., Roberts, D. W., & Roth R. M. (2016). Investigating social cognition in epilepsy using a naturalistic task. Epilepsia, 57, 1515-20.

    Article  PubMed  Google Scholar 

  • Calder, A. J., Keane, J., Manes, F., Antoun, N., & Young, A. W. (2000). Impaired recognition and experience of disgust following brain injury. Nature Neuroscience, 3, 1077-8.

    Article  PubMed  Google Scholar 

  • Calder, A. J., Keane, J., Young, A. W., Lawrence, A. D., Mason, S., & Barker, R. A. (2010). The relation between anger and different forms of disgust: implications for emotion recognition impairments in Huntington’s disease. Neuropsychologia, 48, 2719–2729.

    Article  PubMed  Google Scholar 

  • Caruana, F., Jezzini, A., Sbriscia-Fioretti, B., Rizzolatti, G., & Gallese, V. (2011). Emotional and social behaviors elicited by electrical stimulation of the insula in the macaque monkey. Current Biology, 21, 195-9.

    Article  PubMed  Google Scholar 

  • Chassoux, F., Semah, F., Bouilleret, V., Landre, E., Devaux, B., Turak, B., Nataf, F., & Roux, F.-X. (2004). Metabolic changes and electro-clinical patterns in mesio-temporal lobe epilepsy: a correlative study. Brain, 127, 164-74.

    Article  PubMed  Google Scholar 

  • Chen, C., Lee, Y. H., & Cheng, Y. (2014). Anterior insular cortex activity to emotional salience of voices in a passive oddball paradigm. Frontiers in Human Neuroscience, 8, 743

    Article  PubMed  PubMed Central  Google Scholar 

  • Christopher, L., Koshimori, Y., Lang, A. E., Criaud, M., & Strafella, A. P. (2014). Uncovering the role of the insula in non-motor symptoms of Parkinson’s disease. Brain, 137, 2143-54.

    Article  PubMed  PubMed Central  Google Scholar 

  • Couto, B., Sedeño, L., Sposato, L. A., Sigman, M., Riccio, P M., Salles, A., Lopez, V., Schroeder, J., Manes, F., & Ibanez, A. (2013). Insular networks for emotional processing and social cognition: comparison of two case reports with either cortical or subcortical involvement. Cortex, 49, 1420-34.

    Article  PubMed  Google Scholar 

  • Crespi, C., Cerami, C., Dodich, A., Canessa, N., Arpone, M., Iannaccone, S., Corbo, M., Lunetta, C., Scola, E., Falini, A., & Cappa, S. F. (2014). Microstructural white matter correlates of emotion recognition impairment in Amyotrophic Lateral Sclerosis. Cortex, 53, 1-8.

    Article  PubMed  Google Scholar 

  • de Jong, L. W., Ferrarini, L., van der Grond, J., Milles, J. R., Reiber, J. H., Westendorp, R. G. J., Bollen, E. L. E. M., Middelkoop, H. A. M., & van Buchem, M. A. (2011). Shape abnormalities of the striatum in Alzheimer’s disease. Journal of Alzheimer’s Disease, 23, 49-59.

    Article  PubMed  Google Scholar 

  • Douglas, K. M., & Porter, R. J. (2010). Recognition of disgusted facial expressions in severe depression. British Journal of Psychiatry, 197, 156-7.

    Article  Google Scholar 

  • Draper, A., Jackson, G. M., Morgan, P. S., & Jackson, S. R. (2016). Premonitory urges are associated with decreased grey matter thickness within the insula and sensorimotor cortex in young people with Tourette syndrome. Journal of Neuropsychology, 10, 143-53.

    Article  PubMed  Google Scholar 

  • Drury, H., Channon, S., Barrett, R., Young, M. B., Stern, J. S., Simmons, H., & Crawford, S. (2012). Emotional processing and executive functioning in children and adults with Tourette’s syndrome. Child Neuropsychology, 18, 281-298.

    Article  PubMed  Google Scholar 

  • Dujardin, K., Blairy, S., Defebvre, L., Duhem, S., Noël, Y., Hess, U., & Destée, A. (2004). Deficits in decoding emotional facial expressions in Parkinson’s disease. Neuropsychologia, 42, 239-250.

    Article  PubMed  Google Scholar 

  • Eckart, J. A., Sturm, V. E., Miller, B. L., & Levenson, R. W. (2012). Diminished disgust reactivity in behavioral variant frontotemporal dementia. Neuropsychologia, 50, 786-90.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ekman, P., & Friesen, E. V. (1976). Pictures of facial affect. Consulting Psychologists Press, Palo Alto.

    Google Scholar 

  • Eskildsen, S. F., Coupé, P, Fonov, V. S., Pruessner, J. C., Collins, D. L., & Alzheimer’s Disease Neuroimaging Initiative. (2015). Structural imaging biomarkers of Alzheimer’s disease: predicting disease progression. Neurobiology of Aging, 36 Suppl 1, S23-31.

    Article  PubMed  Google Scholar 

  • Ghosh, B. C. P., Rowe, J. B., Calder, A. J., Hodges, J. R., & Bak, T. H. (2009). Emotion recognition in Progressive Supranuclear Palsy. Journal of Neurology, Neurosurgery and Psychiatry, 80, 1143–1145.

    Article  PubMed  Google Scholar 

  • Gomez-Ibanez, A., Urrestarazu, E., & Viteri, C. (2014). Recognition of facial emotions and identity in patients with mesial temporal lobe and idiopathic generalized epilepsy: An eye-tracking study. Seizure-European Journal of Epilepsy, 23, 892-898.

    Article  PubMed  Google Scholar 

  • Gray, H. M., & Tickle-Degnen, L. (2010). A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychology, 24, 176–91.

    Article  PubMed  Google Scholar 

  • Gurney, K., Prescott, T. J., & Redgrave, P. (2001). A computational model of action selection in the basal ganglia. I. A new functional anatomy. Biological Cybernetics, 84, 401-10.

    Article  PubMed  Google Scholar 

  • Habert, M. O., Lacomblez, L., Maksud, P, El Fakhri, G., Pradat, J. F., & Meininger, V. (2007). Brain perfusion imaging in amyotrophic lateral sclerosis: extent of cortical changes according to the severity and topography of motor impairment. Amyotrophic Lateral Sclerosis, 8, 9-15.

    Article  PubMed  Google Scholar 

  • Hayes, C. J., Stevenson, R. J., & Coltheart, M. (2007). Disgust and Huntington’s disease. Neuropsychologia, 45, 1135–1151.

    Article  PubMed  Google Scholar 

  • Hayes, C. J., Stevenson, R. J., & Coltheart, M. (2009a). The processing of emotion in patients with Huntington’s disease: variability and differential deficits in disgust. Cognitive and Behavioral Neurology, 22, 249–257.

    Article  PubMed  Google Scholar 

  • Hayes, C. J., Stevenson, R. J., & Coltheart, M. (2009b). Production of spontaneous and posed facial expressions in patients with Huntington’s disease: Impaired communication of disgust. Cognition & Emotion, 23, 118–134.

    Article  Google Scholar 

  • Henley, S. M. D., Wild, E. J., Hobbs, N. Z., Warren, J. D., Frost, C., Scahill, R. I., Ridgway, G. R., MacManus, D. G., Barker, R. A., Fox, N. C., & Tabrizi, S. J. (2008). Defective emotion recognition in early HD is neuropsychologically and anatomically generic. Neuropsychologia, 46, 2152–2160.

    Article  PubMed  Google Scholar 

  • Hennion, S., Szurhaj, W., Duhamel, A., Lopes, R., Tyvaert, L., Derambure, P., & Delbeuck, X. (2015). Characterization and prediction of the recognition of emotional faces and emotional bursts in temporal lobe epilepsy. Journal Clinical and Experimental Neuropsychology, 37, 931-945.

    Article  Google Scholar 

  • Henry, J. D., Ruffman, T., McDonald, S., O’Leary, M. A., Phillips, L. H., Brodaty, H., & Rendell P. G. (2008). Recognition of disgust is selectively preserved in Alzheimer’s disease. Neuropsychologia, 46, 1363-70.

    Article  PubMed  Google Scholar 

  • Henry, J. D., Phillips, L. H., Beatty, W. W., McDonald, S., Longley, W. A., Joscelyne, A., & Rendell, P. G. (2009a). Evidence for deficits in facial affect recognition and theory of mind in multiple sclerosis. Journal of the International Neuropsychological Society, 15, 277-85.

    Article  PubMed  Google Scholar 

  • Henry, J. D. P., Rendell, P. G., Scicluna, A., Jackson, M., & Phillips, L. H. (2009b). Emotion Experience, Expression, and Regulation in Alzheimer’s Disease. Psychology and Aging, 24, 252-7.

    Article  PubMed  Google Scholar 

  • Ille, R., Holl, A K., Kapfhammer, H.-P., Reisinger, K., Schäfer, A., & Schienle, A. (2011a). Emotion recognition and experience in Huntington’s disease: is there a differential impairment? Psychiatry Research, 188, 377–82.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ille, R., Schäfer, A., Scharmüller, W., Enzinger, C., Schöggl, H., Kapfhammer, H.-P., & Schienle, A. (2011b). Emotion recognition and experience in Huntington disease: a voxel-based morphometry study. Journal of Psychiatry & Neuroscience, 36, 383–390.

    Article  Google Scholar 

  • Jabbi, M., Bastiaansen, J., & Keysers, C. (2008). A common anterior insula representation of disgust observation, experience and imagination shows divergent functional connectivity pathways. PLoS One, 3, e2939.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jehna, M., Neuper, C., Ischebeck, A., Loitfelder, M., Ropele, S., Langkammer, C., Ebner, F., Fuchs, S., Schmidt, R., Fazekas, F., & Enzinger, C. (2011). The functional correlates of face perception and recognition of emotional facial expressions as evidenced by fMRI. Brain Research, 1393, 73-83.

    Article  PubMed  Google Scholar 

  • Jezzini, A., Caruana, F., Stoianov, I., Gallese, V., & Rizzolatti, G. (2012). Functional organization of the insula and inner perisylvian regions. Proceedings of the National Academy of Science of the United States of America, 109, 10077-82.

    Google Scholar 

  • Josephs, K. A., Whitwell, J. L., Parisi, J. E., & Lapid, M. I. (2016). Coprophagia in neurologic disorders. Journal of Neurology, 263, 1008-1014.

    Article  PubMed  Google Scholar 

  • Kan, Y., Kawamura, M., Hasegawa, Y., Mochizuki, S., & Nakamura, K. (2002). Recognition of emotion from facial, prosodic and written verbal stimuli in Parkinson’s disease. Cortex, 38, 623-630.

    Article  PubMed  Google Scholar 

  • Köchel, A., Schöngassner, F., & Schienle, A. (2013). Cortical activation during auditory elicitation of fear and disgust: a near-infrared spectroscopy (NIRS) study. Neuroscience Letters, 549, 197-200.

    Article  PubMed  Google Scholar 

  • Kotwas, I., Micoulaud-Franchi, J. A., Khalfa, S., McGonigal, A., Bastien-Toniazzo, M., & Bartolomei, F. (2019). Subjective and physiological response to emotions in temporal lobe epilepsy and psychogenic non-epileptic seizures. Journal Affective Disorders, 244, 46-53.

    Article  Google Scholar 

  • Krolak-Salmon, P, Hénaff, M. A., Isnard, J., Tallon-Baudry, C., Guénot, M., Vighetto, A., Bertrand, O., & Mauguière, F. (2003). An attention modulated response to disgust in human ventral anterior insula. Annals of Neurology, 53, 446-53.

    Article  PubMed  Google Scholar 

  • Kumfor, F., Miller, L., Lah, S., Hsieh, S., Savage, S., Hodges, J. R., & Piguet, O. (2011). Are you really angry? The effect of intensity on facial emotion recognition in frontotemporal dementia. Social Neuroscience, 6, 502-14.

    Article  PubMed  Google Scholar 

  • Kumfor, F., Irish, M., Hodges J. R., & Piguet O. (2013). Discrete neural correlates for the recognition of negative emotions: Insights from Frontotemporal Dementia. PLoS One, 8, e67457.

    Article  PubMed  PubMed Central  Google Scholar 

  • Labuschagne, I., Jones, R., Callaghan, J., Whitehead, D., Dumas, E. M., Say, M. J., Hart, E. P., Justo, D., Coleman, A., Santos, R. C. D., Frost, C., Craufurd, D., Tabrizi, S. J., Stout, J. C., & TRACK-HD Investigators (2013). Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington’s disease. Psychiatry Research, 207, 118–126.

    Article  PubMed  Google Scholar 

  • Lavenu, I., & Pasquier, F. (2005). Perception of emotion on faces in frontotemporal dementia and Alzheimer’s disease: a longitudinal study. Dementia and Geriatric Cognitive Disorders, 19, 37-41.

    Article  PubMed  Google Scholar 

  • Lebedev, A. V., Westman, E., Beyer, M. K., Kramberger, M. G., Aguilar, C., Pirtosek, Z., & Aarsland, D. (2013). Multivariate classification of patients with Alzheimer’s and dementia with Lewy bodies using high-dimensional cortical thickness measurements: an MRI surface-based morphometric study. Journal of Neurology, 260, 1104-15.

    Article  PubMed  Google Scholar 

  • Looi, J. C., Walterfang, M., Velakoulis, D., Macfarlane, M. D., Svensson, L. A., & Wahlund, L. O. (2012). Frontotemporal dementia as a frontostriatal disorder: neostriatal morphology as a biomarker and structural basis for an endophenotype. Australian and New Zealand Journal of Psychiatry, 46, 422-34.

    Article  Google Scholar 

  • Lotze, M., Reimold, M., Heymans, U., Laihinen, A., Patt, M., & Halsband, U. (2009). Reduced ventrolateral fMRI response during observation of emotional gestures related to the degree of dopaminergic impairment in Parkinson disease. Journal of Cognitive Neuroscience, 21, 1321-31.

    Article  PubMed  Google Scholar 

  • Lough, S., Kipps, C. M., Treise, C., Watson, P., Blair, J. R., & Hodges, J. R. (2006). Social reasoning, emotion and empathy in frontotemporal dementia. Neuropsychologia, 44, 950-8.

    Article  PubMed  Google Scholar 

  • Madeley, P., Ellis, A. W., & Mindham, R. H. S. (1995). Facial expression and Parkinson’s disease. Behavioral Neurology, 8, 115–119.

    Article  PubMed  Google Scholar 

  • Martin, W. R., Wieler, M., Gee, M., & Camicioli, R. (2009). Temporal lobe changes in early, untreated Parkinson’s disease. Movement Disorders, 20024, 1949-54.

    Article  Google Scholar 

  • Meletti, S., Benuzzi, F., Rubboli, G., Cantalupo, G., Stanzani Maserati, M., Nichelli, P., & Tassinari, C. A. (2003). Impaired facial emotion recognition in early-onset right mesial temporal lobe epilepsy. Neurology, 60, 426-31.

    Article  PubMed  Google Scholar 

  • Meletti S., Benuzzi F., Cantalupo G., Rubboli G., Tassinari C. A., & Nichelli P. (2009). Facial emotion recognition impairment in chronic temporal lobe epilepsy. Epilepsia, 50, 1547-59.

    Article  PubMed  Google Scholar 

  • Mermillod, M., Devaux, D., Derost, P., Rieu, I., Chambres, P., Auxiette, C., Legrand, G., Galland, F., Dalens, H., Coulangeon, L. M., Broussolle, E., Durif, F., & Jalenques, I. (2013). Rapid presentation of emotional expressions reveals new emotional impairments in Tourette’s syndrome. Frontiers in Human Neuroscience, 7, 149.

    Article  PubMed  PubMed Central  Google Scholar 

  • Milders, M., Crawford, J. R., Lamb, A., & Simpson, S. A. (2003). Differential deficits in expression recognition in gene-carriers and patients with Huntington’s disease. Neuropsychologia, 41, 1484–1492.

    Article  PubMed  Google Scholar 

  • Moran, N. F., Lemieux, L., Kitchen, N. D., Fish, D. R., & Shorvon, S. D. (2001). Extrahippocampal temporal lobe atrophy in temporal lobe epilepsy and mesial temporal sclerosis. Brain, 124, 167-75.

    Article  PubMed  Google Scholar 

  • Mufson, E. J., & Mesulam, M. M. (1982). Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum. Journal of Comparative Neurology, 212, 23-37.

    Google Scholar 

  • Nopoulos, P. C., Aylward, E. H., Ross, C. A., Johnson, H. J., Magnotta, V. A., Juhl, A. R., Pierson, R. K., Mills, J., Langbehn, D. R., Paulsen, J. S., & the PREDICT-HD Investigators and Coordinators of the Huntington Study Group (HSG) (2010). Cerebral cortex structure in prodromal Huntington Disease. Neurobiology of Disease, 40, 544–554.

    Article  PubMed  PubMed Central  Google Scholar 

  • Obeso, J. A., Rodriguez-Oroz, M. C., Rodriguez, M., Lanciego, J. L., Artieda, J., Gonzalo, N., & Olanow, C. W. (2000). Pathophysiology of the basal ganglia in Parkinson’s disease. Trends in Neurosciences, 23, S8–S19.

    Article  PubMed  Google Scholar 

  • Oh, S. I., Oh, K. W., Kim, H. J., Park, J. S., & Kim, S. H. (2016). Impaired Perception of Emotional Expression in Amyotrophic Lateral Sclerosis. Journal of Clinical Neurology, 12, 295-300.

    Article  PubMed  PubMed Central  Google Scholar 

  • Oliver, L. D., Virani, K., Finger, E. C., & Mitchell, D. G. (2014). Is the emotion recognition deficit associated with frontotemporal dementia caused by selective inattention to diagnostic facial features? Neuropsychologia, 60, 84-92.

    Article  PubMed  Google Scholar 

  • Orbach, L., Menascu, S., Hoffmann, C., Miron, S., & Achiron, A. (2018). Focal cortical thinning in patients with stable relapsing-remitting multiple sclerosis: cross-sectional-based novel estimation of gray matter kinetics. Neuroradiology, 60, 179-187.

    Article  PubMed  Google Scholar 

  • Otero, M. C., & Levenson, R. W. (2019). Emotion regulation via visual avoidance: Insights from neurological patients. Neuropsychologia, 131, 91-101.

    Article  PubMed  PubMed Central  Google Scholar 

  • Park, S., Kim, T, Shin, S. A., Kim, Y. K., Sohn, B. K., Park, H. J., Youn, J. H., & Lee, J. Y. (2017). Behavioral and Neuroimaging Evidence for Facial Emotion Recognition in Elderly Korean Adults with Mild Cognitive Impairment, Alzheimer’s Disease, and Frontotemporal Dementia. Frontiers in Aging Neuroscience, 9, 389.

    Article  PubMed  PubMed Central  Google Scholar 

  • Philippi, N., Kemp, J., Constans-Erbs, M., Hamdaoui, M., Monjoin, L., Ehrhard, E., Albasser, T., Botzung, A., Demuynck, C., Heim, G., Martin-Hunyadi, C., Bilger, M., Berly, L., Soulier, D., Cretin, B., Despres, O., & Blanc, F. (2017). Insular cognitive impairment at the early stage of dementia with Lewy bodies: a preliminary study. Gériatrie et Psychologie Neuropsychiatrie du Vieillissement, 15, 329-338.

    Article  PubMed  Google Scholar 

  • Phillips, M. L., Young, A. W., Senior, C., Brammer, M., Andrew, C., Calder, A. J., Bullmore, E. T., Perrett, D. I., Rowland, D., Williams, S. C., Gray, J. A., & David, A. S. (1997). A specific neural substrate for perceiving facial expressions of disgust. Nature, 389, 495-8.

    Article  PubMed  Google Scholar 

  • Phillips, M. L., Young, A. W., Scott, S. K., Calder, A. J., Andrew, C., Giampietro, V., Williams, S. C., Bullmore, E. T., Brammer, M., & Gray, J. A. (1998). Neural responses to facial and vocal expressions of fear and disgust. Proceedings of the Royal Society B, 265, 1809-17.

    Google Scholar 

  • Prochnow, D, Donell, J., Schaefer, R., Jorgens, S., Hartung, H. P., Franz, M., & Seitz, R. J. (2011). Alexithymia and impaired facial affect recognition in multiple sclerosis. Journal of Neurology, 258, 1683-1688.

    Article  PubMed  Google Scholar 

  • Pujol, J., Blanco-Hinojo, L., Coronas, R., Esteba-Castillo, S., Rigla, M., Martínez-Vilavella, G., Deus, J., Novell, R., & Caixàs, A. (2018). Mapping the sequence of brain events in response to disgusting food. Human Brain Mapping, 2039, 369-380.

    Article  Google Scholar 

  • Redgrave, P., Prescott, T. J., & Gurney, K. (1999). The basal ganglia: a vertebrate solution to the selection problem? Neuroscience, 89, 1009-23.

    Article  PubMed  Google Scholar 

  • Reep, R. L., & Winans, S. S. (1982). Afferent connections of dorsal and ventral agranular insular cortex in the hamster Mesocricetus auratus. Neuroscience, 7, 1265-88.

    Article  PubMed  Google Scholar 

  • Rees, E. M., Farmer, R., Cole, J. H., Henley, S. M. D., Sprengelmeyer, R., Frost, C., Scahill, R. I., Hobbs, N. Z., & Tabrizi, S. J. (2014). Inconsistent emotion recognition deficits across stimulus modalities in Huntington′s disease. Neuropsychologia, 64, 99–104.

    Article  PubMed  Google Scholar 

  • Robotham, L., Sauter, D. A., Bachoud-Levi, A. C., Trinkler, I., Bachoud-Lévi, A.-C., & Trinkler, I. (2011). The impairment of emotion recognition in Huntington’s disease extends to positive emotions. Cortex, 47, 880–884.

    Article  PubMed  Google Scholar 

  • Rosas, H. D., Salat, D. H., Lee, S. Y., Zaleta, A K., Pappu, V., Fischl, B, Greve, D., Hevelone, N., & Hersch, S. M. (2008). Cerebral cortex and the clinical expression of Huntington’s disease: complexity and heterogeneity. Brain, 131, 1057–1068.

    Article  PubMed  Google Scholar 

  • Sambataro, F., Dimalta, S., Di Giorgio, A., Taurisano, P., Blasi, G., Scarabino, T., Giannatempo, G., Nardini, M., & Bertolino, A. (2006). Preferential responses in amygdala and insula during presentation of facial contempt and disgust. European Journal of Neuroscience, 24, 2355-62.

    Article  Google Scholar 

  • Sapey-Triomphe, L. A., Heckemann, R. A., Boublay, N., Dorey, J. M., Hénaff, M. A., Rouch, I., Padovan, C., Hammers, A., Krolak-Salmon, P., & Alzheimer’s Disease Neuroimaging Initiative. (2015). Neuroanatomical correlates of recognizing face expressions in mild stages of Alzheimer’s disease. PLoS One, 10, e0143586.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sedda, A., Rivolta, D., Scarpa, P., Burt, M., Frigerio, E., Zanardi, G., Piazzini, A., Turner, K., Canevini, M. P., Francione, S., Russo, G. L., & Bottini, G. (2013). Ambiguous emotion recognition in temporal lobe epilepsy: the role of expression intensity. Cognitive, Affective, and Behavioral Neuroscience, 13, 452-63.

    Article  Google Scholar 

  • Shimizu, H., & Norita, M. (1991). Connections of the insular cortex in kittens: an anatomical demonstration with wheatgerm agglutinin conjugated to horseradish peroxidase technique. International Journal of Developmental Neuroscience, 9, 479-91.

    Article  PubMed  Google Scholar 

  • Simons, G., Pasqualini, M. C., Reddy, V., & Wood, J. (2004). Emotional and non emotional facial expressions in people with Parkinson’s disease. Journal of the International Neuropsychology Society, 10, 521–555.

    Article  Google Scholar 

  • Smith, M. C., Smith, M. K., & Ellgring, H. (1996). Spontaneous and posed facial expression in Parkinson’s disease. Journal of the International Neuropsychology Society, 2, 383–391.

    Article  Google Scholar 

  • Snowden, J. S., Austin, N. A., Sembi, S., Thompson, J. C., Craufurd, D., & Neary, D. (2008). Emotion recognition in Huntington’s disease and frontotemporal dementia. Neuropsychologia, 46, 2638–2649.

    Article  PubMed  Google Scholar 

  • Sprengelmeyer, R., Young, A. W., Calder, A. J., Karnat, A., Lange, H., Homberg, V., Perrett, D. I., & Rowland, D. (1996). Loss of disgust. Perception of faces and emotions in Huntington’s disease. Brain, 119, 1647–1665.

    Google Scholar 

  • Sprengelmeyer, R., Young, A. W., Pundt, I., Sprengelmeyer, A., Calder, A. J., Berrios, G., Winkel, R., Vollmoeller, W., Kuhn, W., Sartory, G., & Przuntek, H. (1997). Disgust implicated in Obsessive-Compulsive Disorder. Proceedings of the Royal Society B, 264, 1767–1773.

    Google Scholar 

  • Sprengelmeyer, R., Young, A. W., Mahn, K., Schroeder, U., Woitalla, D., Büttner, T, Kuhn, W., & Przuntek, H. (2003). Facial expression recognition in people with medicated and unmedicated Parkinson’s disease. Neuropsychologia, 41, 1047-1057.

    Article  PubMed  Google Scholar 

  • Straube, T, Weisbrod, A., Schmidt, S., Raschdorf, C., Preul, C., Mentzel, H. J., & Miltner, W. H. (2010). No impairment of recognition and experience of disgust in a patient with a right-hemispheric lesion of the insula and basal ganglia. Neuropsychologia, 48, 1735-41.

    Article  PubMed  Google Scholar 

  • Suzuki, A., Hoshino, T., Shigemasu, K., & Kawamura, M. (2006). Disgust-specific impairment of facial expression recognition in Parkinson’s disease. Brain, 129, 707–717.

    Article  PubMed  Google Scholar 

  • Trinkler, I., de Langavant, L. C., & Bachoud-Levi, A. C. (2013). Joint recognition-expression impairment of facial emotions in Huntington’s disease despite intact understanding of feelings. Cortex, 49, 549–558.

    Article  PubMed  Google Scholar 

  • Tsatali, M., Overton, P. G., & Vivas, A. B. (2019). Self-reported and experimentally induced self-disgust is heightened in Parkinson’s disease: Contribution of behavioural symptoms. PLoS One, 14, e0223663.

    Article  PubMed  PubMed Central  Google Scholar 

  • Verstaen, A., Eckart, J. A., Muhtadie, L., Otero, M. C., Sturm, V. E., Haase, C. M., Miller, B. L., & Levenson, R. W. (2016). Insular atrophy and diminished disgust reactivity. Emotion, 16, 903-12.

    Article  PubMed  PubMed Central  Google Scholar 

  • von dem Hagen, E. A., Beaver, J. D., Ewbank, M. P., Keane, J., Passamonti, L., Lawrence, A. D., & Calder, A. J. (2009). Leaving a bad taste in your mouth but not in my insula. Social Cognitive and Affective Neuroscience, 4, 379-86.

    Article  Google Scholar 

  • Wang K., Hoosain, R., Yang, R.-M. M., Meng, Y., & Wang, C.-Q. Q. (2003). Impairment of recognition of disgust in Chinese with Huntington’s or Wilson’s disease. Neuropsychologia, 41, 527–537.

    Article  PubMed  Google Scholar 

  • Whitwell, J. L., Przybelski, S. A., Weigand, S. D., Ivnik, R J., Vemuri, P., Gunter, J. L., Senjem, M. L., Shiung, M. M, Boeve, B. F., Knopman, D. S., Parisi, J. E., Dickson, D. W., Petersen, R. C., Jack Jr, C. R., & Josephs, K. A. (2009). Distinct anatomical subtypes of the behavioural variant of frontotemporal dementia: a cluster analysis study. Brain, 132, 2932-46.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wicker, B., Keysers, C., Plailly, J., Royet, J. P, Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust. Neuron, 40, 655-64.

    Article  PubMed  Google Scholar 

  • Wright, P., He, G., Shapira, N. A., Goodman, W. K., & Liu, Y. (2004). Disgust and the insula: fMRI responses to pictures of mutilation and contamination. Neuroreport, 15, 2347-51.

    Article  PubMed  Google Scholar 

  • Zamboni, G., Grafman, J., Krueger, F., Knutson, K. M., & Huey, E. D. (2010). Anosognosia for behavioral disturbances in frontotemporal dementia and corticobasal syndrome: A voxel-based morphometry study. Dementia and Geriatric Cognitive Disorders, 29, 88-96.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zarotti, N., Fletcher, I., & Simpson, J. (2019). New perspectives on emotional processing in people with symptomatic Huntington’s disease: impaired emotion regulation and recognition of emotional body language. Archives of Clinical Neuropsychology, 34, 610-624.

    Article  PubMed  Google Scholar 

  • Zimmerman, E. K., Eslinger, P. J., Simmons, Z., & Barrett, A. M. (2007). Emotional perception deficits in amyotrophic lateral sclerosis. Cognitive and Behavioral Neurology, 20, 79-82.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the contribution of Dr. Nicolo Zarotti for his input relating to the data on Huntington’s disease, and Dr. Marianna Tsatali for her input relating to the data on Parkinson’s disease.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul G. Overton .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Overton, P.G., Vivas, A.B., Simpson, J. (2021). Disgust in Neurological Disorders. In: Powell, P.A., Consedine, N.S. (eds) The Handbook of Disgust Research. Springer, Cham. https://doi.org/10.1007/978-3-030-84486-8_12

Download citation

Publish with us

Policies and ethics