Skip to main content Accessibility help

Apathy Associated With Impaired Recognition of Happy Facial Expressions in Huntington’s Disease

  • Katherine Osborne-Crowley (a1), Sophie C. Andrews (a2), Izelle Labuschagne (a3), Akshay Nair (a1), Rachael Scahill (a1), David Craufurd (a4) (a5), Sarah J. Tabrizi (a1), Julie C. Stout (a2) and the TRACK-HD Investigators (a1) (a2) (a3) (a4) (a5)...

Objectives: Previous research has demonstrated an association between emotion recognition and apathy in several neurological conditions involving fronto-striatal pathology, including Parkinson’s disease and brain injury. In line with these findings, we aimed to determine whether apathetic participants with early Huntington’s disease (HD) were more impaired on an emotion recognition task compared to non-apathetic participants and healthy controls. Methods: We included 43 participants from the TRACK-HD study who reported apathy on the Problem Behaviours Assessment – short version (PBA-S), 67 participants who reported no apathy, and 107 controls matched for age, sex, and level of education. During their baseline TRACK-HD visit, participants completed a battery of cognitive and psychological tests including an emotion recognition task, the Hospital Depression and Anxiety Scale (HADS) and were assessed on the PBA-S. Results: Compared to the non-apathetic group and the control group, the apathetic group were impaired on the recognition of happy facial expressions, after controlling for depression symptomology on the HADS and general disease progression (Unified Huntington’s Disease Rating Scale total motor score). This was despite no difference between the apathetic and non-apathetic group on overall cognitive functioning assessed by a cognitive composite score. Conclusions: Impairment of the recognition of happy expressions may be part of the clinical picture of apathy in HD. While shared reliance on frontostriatal pathways may broadly explain associations between emotion recognition and apathy found across several patient groups, further work is needed to determine what relationships exist between recognition of specific emotions, distinct subtypes of apathy and underlying neuropathology. (JINS, 2019, 00, 1–9)

Corresponding author
Correspondence and reprint requests to: Katherine Osborne-Crowley, Huntington’s Disease Centre, University College London, Institute of Neurology, and National Hospital for Neurology and Neurosurgery, London, UK. E-mail:
Hide All

TRACK-HD Investigators: Australia—C. Campbell, M. Campbell, E. Frajman, C. Milchman, A. O’Regan (Monash University, Victoria). Canada—A. Coleman, R. Dar Santos, J. Decolongon, A. Sturrock (University of British Columbia, Vancouver). France—E. Bardinet, C. Jauffret, D. Justo, S. Lehericy, C. Marelli, K. Nigaud, P. Pourchot, R. Valabrègue (APHP, Hôpital Salpêtriere, Paris). Germany—N. Bechtel, S. Bohlen, R. Reilmann (University of Münster, Münster); A. Hoffman, P. Kraus (University of Bochum, Bochum); B. Landwehrmeyer (University of Ulm). Netherlands—S.J.A. van den Bogaard, E.M. Dumas, J. van der Grond, E.P. t’Hart, C. Jurgens, M.-N. Witjes-Ane (Leiden University Medical Centre, Leiden). United Kingdom—N. Arran, J. Callaghan, C. Stopford (St Mary’s Hospital, Manchester); C. Frost, R. Jones (London School of Hygiene and Tropical Medicine, London); C. Berna, H. Crawford, N. Fox, C. Gibbard, N. Hobbs, N. Lahiri, I. Malone, R. Ordidge, G. Owen, A. Patel, T. Pepple, J. Read, M. Say, R. Scahill, D. Whitehead, E. Wild (University College London, London); S. Keenan (Imperial College London, London); D.M. Cash (IXICO, London); S. Hicks, C. Kennard (Oxford). United States—T. Acharya, E. Axelson, H. Johnson, D. Langbehn, C. Wang (University of Iowa, Iowa City, IA); S. Lee, W. Monaco, H. Rosas (Massachusetts General Hospital, Harvard, MA); C. Campbell, S. Queller, K. Whitlock (Indiana University, IN); B. Borowsky, A. Tobin (CHDI).

Hide All
Aarsland, D., Larsen, J.P., Lim, N.G., Janvin, C., Karlsen, K., Tandberg, E., & Cummings, J.L. (1999). Range of neuropsychiatric disturbances in patients with Parkinson’s disease. Journal of Neurology, Neurosurgery, & Psychiatry, 67(4), 492496.
Aarsland, D., Litvan, I., & Larsen, J.P. (2001). Neuropsychiatric symptoms of patients with progressive supranuclear palsy and Parkinson’s disease. The Journal of Neuropsychiatry and Clinical Neurosciences, 13(1), 4249.
Adolphs, R. (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12, 169177.
Adolphs, R., Tranel, D., & Damasio, A.R. (2003). Dissociable neural systems for recognizing emotions. Brain and Cognition, 52(1), 6169.
Bhatia, K.P., & Marsden, C.D. (1994). The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain, 117, 859876.
Bora, E., Velakoulis, D., & Walterfang, M. (2016). Social cognition in Huntington’s disease: A meta-analysis. Behavioural Brain Research, 297, 131140.
Buunk, A.M., Spikman, J.M., Veenstra, W.S., van Laar, P.J., Metzemaekers, J.D.M., van Dijk, J.M.C., … Groen, R.J.M. (2017). Social cognition impairments after aneurysmal subarachnoid haemorrhage: Associations with deficits in interpersonal behaviour, apathy, and impaired self-awareness. Neuropsychologia, 103, 131139.
Callaghan, J., Stopford, C., Arran, N., Boisse, M.-F., Coleman, A., Santos, R.D., … Craufurd, D. (2015). Reliability and factor structure of the short problem behaviors assessment for Huntington’s Disease (PBA-s) in the TRACK-HD and REGISTRY studies. The Journal of Neuropsychiatry and Clinical Neurosciences, 27(1), 5964.
Camacho, M., Barker, R., & Mason, S.L. (2018). Apathy in Huntington’s disease: A review of the current conceptualisation. Journal of Alzheimer’s Disease and Parkinsonism, 8(20), doi:10.4172/2161-0460.1000431
Cowan, N., Elliott, E.M., Saults, S.J., Morey, C.C., Mattox, S., Hismjatullina, A., & Conway, A.R.A. (2005). On the capacity of attention: Its estimation and its role in working memory and cognitive aptitudes. Cognitive Psychology, 61, 41100.
Craufurd, D., Thompson, J.C., & Snowden, J.S. (2001). Behavioral changes in Huntington Disease. Neuropsychiatry, Neuropsychology, and Behavioral Neurology, 14(4), 219226.
Dalili, M.N., Penton-Voak, I.S., Harmer, C.J., & Munaf, M.R. (2015). Meta-analysis of emotion recognition deficits in major depressive disorder. Psychological Medicine, 45(6), 11351144.
Delmaire, C., Dumas, E.M., Sharman, M.A., van den Bogaard, S.J.A., Valabregue, R., Jauffret, C., … Lehéricy, S. (2013). The structural correlates of functional deficits in early huntington’s disease. Human Brain Mapping, 34(9), 21412153.
Drapier, D., Drapier, S., Sauleau, P., Haegelen, C., Raoul, S., Biseul, I., … Millet, B. (2006). Does subthalamic nucleus stimulation induce apathy in Parkinson’s disease? Journal of Neurology, 253(8), 10831091.
Eddy, C.M., & Rickards, H.E. (2013). Impact of cognitive and behavioural changes on quality of life in Huntington’s disease. Basal Ganglia, 3(2), 123126.
Ekman, P., & Friesen, W.V. (1976). Pictures of facial affect. Paulo Alto: Consulting Psychologists Press.
Engelborghs, S., Marien, P., Pickut, B.A., Verstraeten, S., & De Deyn, P.P. (2000). Loss of psychic self-activation after paramedian bithalamic infarction. Stroke, 31(7), 17621765.
Eslinger, P.J., & Damasio, A.R. (1985). Severe disturbance of higher cognition after bilateral frontal lobe ablation: Patient EVR. Neurology, 35(12), 17311731.
Fritz, N.E., Boileau, N.R., Stout, J.C., Ready, R., Perlmutter, J.S., Paulsen, J.S., … Carlozzi, N.E. (2018). Relationships among apathy, health-related quality of life, and function in Huntington’s disease. The Journal of Neuropsychiatry and Clinical Neurosciences, 30(3), 194201.
Ghika-Schmid, F., & Bogousslavsky, J. (2000). The acute behavioral syndrome of anterior thalamic infarction: A prospective study of 12 cases. Annals of Neurology, 48(2), 220227.<220::AID-ANA12>3.0.CO;2-M
Golden, C.J. (1978). Stroop Color and Word Test: Manual for clinical and experimental uses. Chicago: Stoetling.
Hamilton, J.M., Salmon, D.P., Corey-Bloom, J., Gamst, A., Paulsen, J.S., Jerkins, S., … Peavy, G. (2003). Behavioural abnormalities contribute to functional decline in Huntington’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 74(1), 120122.
Henley, S.M., Novak, M.J., Frost, C., King, J., Tabrizi, S.J., & Warren, J.D. (2012). Emotion recognition in Huntington’s disease: A systematic review. Neuroscience and Biobehavioral Reviews, 36, 237253.
Henley, S.M., Wild, E.J., Hobbs, N.Z., Warren, J.D., Frost, C., Scahill, R.I., … Tabrizi, S.J. (2008). Defective emotion recognition in early HD is neuropsychologically and anatomically generic. Neuropsychologia, 46(8), 21522160.
Ille, R., Schäfer, A., Scharmüller, W., Enzinger, C., Schöggl, H., Kapfhammer, H.-P., & Schienle, A. (2011). Emotion recognition and experience in Huntington disease: A voxel-based morphometry study. Journal of Psychiatry & Neuroscience, 36(6), 383390.
Ioannidis, A.E., Kimiskidis, V.K., Loukopoulou, E., Geroukis, T., Vlaikidis, N., & Kosmidis, M.H. (2013). Apathy, cognitive dysfunction and impaired social cognition in a patient with bilateral thalamic infarction. Neurocase, 19(5), 513520.
Isella, V., Melzi, P., Grimaldi, M., Iurlaro, S., Piolti, R., Ferrarese, C., … Appollonio, I. (2002). Clinical, neuropsychological, and morphometric correlates of apathy in Parkinson’s disease. Movement Disorders, 17(2), 366371.
Jacobs, M., Hart, E.P., & Roos, R. (2018). Cognitive performance and apathy predict unemployment in Huntington’s disease mutation carriers. The Journal of Neuropsychiatry and Clinical Neurosciences, 30, 188193. doi:10.1176/appi.neuropsych.17070144
Kempnich, C.L., Andrews, S.C., Fisher, F., Wong, D., Georgiou-Karistianis, N., & Stout, J.C. (2017). Emotion recognition correlates with social-neuropsychiatric dysfunction in Huntington’s disease. Journal of the International Neuropsychological Society, (2017), 17.
Kordsachia, C.C., Labuschagne, I., & Stout, J.C. (2017). Beyond emotion recognition deficits: A theory guided analysis of emotion processing in Huntington’s disease. Neuroscience and Biobehavioral Reviews, 73, 276292.
Levy, R., & Dubois, B. (2006). Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cerebral Cortex, 16, 916928.
Litvan, I., Paulsen, J.S., Mega, M.S., & Cummings, J.L. (1998). Neuropsychiatric assessment of patients with hyperkinetic and hypokinetic movement disorders. Archives of Neurology, 55(10), 13131319.
Martínez-Corral, M., Pagonabarraga, J., Llebaria, G., Pascual-Sedano, B., García-Sánchez, C., Gironell, A., & Kulisevsky, J. (2010). Facial emotion recognition impairment in patients with Parkinson’s disease and isolated apathy. Parkinson’s Disease, 2010, 15.
Moretti, R., & Signori, R. (2016). Neural correlates for apathy: Frontal-prefrontal and parietal cortical-subcortical circuits. Frontiers in Aging Neuroscience, 8, 289.
Njomboro, P., & Deb, S. (2014). Distinct neuropsychological correlates of cognitive, behavioral, and affective apathy sub-domains in acquired brain injury. Frontiers in Neurology, 5, 73.
Njomboro, P., Humphreys, G.W., & Deb, S. (2014). Exploring social cognition in patients with apathy following acquired brain damage. BMC Neurology, 14(1), 18.
Paulsen, J.S., Miller, A.C., Hayes, T., & Shaw, E. (2017). Cognitive and behavioral changes in Huntington disease before diagnosis. Handbook of Clinical Neurology, 144, 6991. doi:10.1016/B978-0-12-801893-4.00006-7
Penney, J.B., Vonsattel, J.P., MacDonald, M.E., Gusella, J.F., & Myers, R.H. (1997). CAG repeat number governs the development rate of pathology in Huntington’s disease. Annals of Neurology, 41(5), 689692.
Pluck, G.C., & Brown, R.G. (2002). Apathy in Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 73(6), 636642.
Reitan, R.M. (1955). The relation of the Trail Making Test to organic brain damage. Journal of Consulting Psychology, 19(5), 393394.
Robert, G., Le Jeune, F., Dondaine, T., Drapier, S., Péron, J., Lozachmeur, C., … Drapier, D. (2014). Apathy and impaired emotional facial recognition networks overlap in Parkinson’s disease: A PET study with conjunction analyses. Journal of Neurology, Neurosurgery, and Psychiatry, 85(10), 11531158.
Rolls, E.T. (2000). The orbitofrontal cortex and reward. Cerebral Cortex, 10(3), 284294.
Rosenberg, H., McDonald, S., Dethier, M., Kessels, R.P.C., & Westbrook, R.F. (2014). Facial emotion recognition deficits following moderate-severe traumatic brain injury (TBI): Re-examining the valence effect and the role of emotion intensity. Journal of the International Neuropsychological Society, 20(10), 9941003.
Ruff, C.C., & Fehr, E. (2014). The neurobiology of rewards and values in social decision making. Nature Reviews Neuroscience, 15(8), 549562.
Scahill, R.I., Hobbs, N.Z., Jones, R., Frost, C., Reilmann, R., Bechtel, N., & Hicks, S.L. (2009). Correlations between structural loss and functional decline in premanifest and early Huntington’s disease: Cross-sectional Vbm analysis from Track-hd. Clinical Genetics, 76, 44.
Schroeder, U. (2004). Facial expression recognition and subthalamic nucleus stimulation. Journal of Neurology, Neurosurgery, & Psychiatry, 75(4), 648650.
Shoulson, I., & Fahn, S. (1979). Huntington disease: Clinical care and evaluation. Neurology, 29(1), 13.
Simpson, J.A., Lovecky, D., Kogan, J., Vetter, L.A., & Yohrling, G.J. (2016). Survey of the Huntington’s disease patient and caregiver community reveals most impactful symptoms and treatment needs. Journal of Huntington’s Disease, 5, 395403.
Smith, A. (1982). Symbol digit modalities test. Los Angeles, CA: Western Psychological Services.
Stout, J.C., Tomusk., A., Queller, S., Lifer, S., Hastings, S., Dawson, J., … Johnson, S. (2008). Optimal measurement of clinical and bioligcal markers for clinical trials: The HD Toolkit Project. Neurotherapeutics, 5(2), 362375.
Stout, J.C., Paulsen, J.S., Queller, S., Solomon, A.C., Whitlock, K.B., Campbell, J.C., … Aylward, E.H. (2011). Neurocognitive signs in prodromal Huntington disease. Neuropsychology, 25(1), 114.
Stuss, D.T., Van Reekum, R., & Murphy, K.J. (2000). Differentiation of states and causes of apathy. In: The neuropsychology of emotion (pp. 340363). Retrieved from
Tabrizi, S.J., Langbehn, D.R., Leavitt, B.R., Roos, R.A., Durr, A., Craufurd, D., … Stout, J.C. (2009). Biological and clinical manifestations of Huntington’s disease in the longitudinal TRACK-HD study: Cross-sectional analysis of baseline data. The Lancet Neurology, 8(9), 791801.
van Duijn, E., Craufurd, D., Hubers, A.A., Giltay, E.J., Bonelli, R., Rickards, H., … European Huntington’s Disease Network Behavioural Phenotype Working Group. (2014). Neuropsychiatric symptoms in a European Hintington’s disease cohort (REGISTRY). Journal of Neurology, Neurosurgery, and Psychiatry, 85, 14111418.
Zigmond, A.S., & Snaith, R.P. (1983). The Hospital Anxiety and Depression Scale. Acta Psychiatrica Scandinavica, 67(6), 361370.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the International Neuropsychological Society
  • ISSN: 1355-6177
  • EISSN: 1469-7661
  • URL: /core/journals/journal-of-the-international-neuropsychological-society
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed