Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-25T05:56:22.606Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  15 February 2019

Katherine Osborne-Crowley ,
Sophie C. Andrews ,
Izelle Labuschagne ,
Akshay Nair ,
Rachael Scahill ,
David Craufurd ,
Sarah J. Tabrizi ,
Julie C. Stout Open the ORCID record for Julie C. Stout [Opens in a new window]  and
the TRACK-HD Investigators
Katherine Osborne-Crowley*
Affiliation:
Huntington’s Disease Centre, University College London, Institute of Neurology, and National Hospital for Neurology and Neurosurgery, London, United Kingdom
Sophie C. Andrews
Affiliation:
Monash Institute of Cognitive and Clinical Neurosciences, School of Psychological Sciences, Monash University, Melbourne, Australia
Izelle Labuschagne
Affiliation:
Cognition and Emotion Research Centre, School of Psychology, Australian Catholic University, Melbourne, Australia
Akshay Nair
Affiliation:
Huntington’s Disease Centre, University College London, Institute of Neurology, and National Hospital for Neurology and Neurosurgery, London, United Kingdom
Rachael Scahill
Affiliation:
Huntington’s Disease Centre, University College London, Institute of Neurology, and National Hospital for Neurology and Neurosurgery, London, United Kingdom
David Craufurd
Affiliation:
Manchester Centre for Genomic Medicine, Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom St. Mary’s Hospital, Central Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, United Kingdom
Sarah J. Tabrizi
Affiliation:
Huntington’s Disease Centre, University College London, Institute of Neurology, and National Hospital for Neurology and Neurosurgery, London, United Kingdom
Julie C. Stout
Affiliation:
Monash Institute of Cognitive and Clinical Neurosciences, School of Psychological Sciences, Monash University, Melbourne, Australia
the TRACK-HD Investigators
Affiliation:
Huntington’s Disease Centre, University College London, Institute of Neurology, and National Hospital for Neurology and Neurosurgery, London, United Kingdom Monash Institute of Cognitive and Clinical Neurosciences, School of Psychological Sciences, Monash University, Melbourne, Australia Cognition and Emotion Research Centre, School of Psychology, Australian Catholic University, Melbourne, Australia Manchester Centre for Genomic Medicine, Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom St. Mary’s Hospital, Central Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, United Kingdom
*
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: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

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, 25, 453–461)

Keywords

Huntington’s diseaseEmotionApathySocial behaviorCognitionCognition disorders
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 5 , May 2019 , pp. 453 - 461
Copyright
Copyright © The International Neuropsychological Society 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

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).

References

REFERENCES

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), 492–496. https://doi.org/10.1136/jnnp.67.4.492 CrossRefGoogle ScholarPubMed
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), 42–49. https://doi.org/10.1176/jnp.13.1.42b CrossRefGoogle ScholarPubMed
Adolphs, R. (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12, 169–177. https://doi.org/10.1016/S0959-4388(02)00301-X CrossRefGoogle ScholarPubMed
Adolphs, R., Tranel, D., & Damasio, A.R. (2003). Dissociable neural systems for recognizing emotions. Brain and Cognition, 52(1), 61–69. https://doi.org/10.1016/S0278-2626(03)00009-5 CrossRefGoogle ScholarPubMed
Bhatia, K.P., & Marsden, C.D. (1994). The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain, 117, 859–876.CrossRefGoogle ScholarPubMed
Bora, E., Velakoulis, D., & Walterfang, M. (2016). Social cognition in Huntington’s disease: A meta-analysis. Behavioural Brain Research, 297, 131–140. https://doi.org/10.1016/j.bbr.2015.10.001 CrossRefGoogle ScholarPubMed
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, 131–139. https://doi.org/10.1016/j.neuropsychologia.2017.07.015 CrossRefGoogle ScholarPubMed
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), 59–64. https://doi.org/10.1176/appi.neuropsych.13070169 CrossRefGoogle ScholarPubMed
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:10.4172/2161-0460.1000431CrossRefGoogle Scholar
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, 41–100. https://doi.org/10.1016/j.cogpsych.2004.12.001 Google Scholar
Craufurd, D., Thompson, J.C., & Snowden, J.S. (2001). Behavioral changes in Huntington Disease. Neuropsychiatry, Neuropsychology, and Behavioral Neurology, 14(4), 219–226.Google ScholarPubMed
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), 1135–1144. https://doi.org/10.1017/S0033291714002591 CrossRefGoogle ScholarPubMed
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), 2141–2153. https://doi.org/10.1002/hbm.22055 CrossRefGoogle ScholarPubMed
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), 1083–1091. https://doi.org/10.1007/s00415-006-0177-0 CrossRefGoogle ScholarPubMed
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), 123–126.CrossRefGoogle Scholar
Ekman, P., & Friesen, W.V. (1976). Pictures of facial affect. Paulo Alto: Consulting Psychologists Press.Google Scholar
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), 1762–1765. https://doi.org/10.1161/01.STR.31.7.1762 CrossRefGoogle ScholarPubMed
Eslinger, P.J., & Damasio, A.R. (1985). Severe disturbance of higher cognition after bilateral frontal lobe ablation: Patient EVR. Neurology, 35(12), 1731–1731. https://doi.org/10.1212/WNL.35.12.1731 CrossRefGoogle ScholarPubMed
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), 194–201.CrossRefGoogle ScholarPubMed
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), 220–227. https://doi.org/10.1002/1531-8249(200008)48:2<220::AID-ANA12>3.0.CO;2-M 3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Golden, C.J. (1978). Stroop Color and Word Test: Manual for clinical and experimental uses. Chicago: Stoetling.Google Scholar
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), 120–122. https://doi.org/10.1136/jnnp.74.1.120 CrossRefGoogle ScholarPubMed
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, 237–253. https://doi.org/10.1016/j.neubiorev.2011.06.002 CrossRefGoogle ScholarPubMed
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), 2152–2160. https://doi.org/10.1016/j.neuropsychologia.2008.02.025 CrossRefGoogle ScholarPubMed
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), 383–390. https://doi.org/10.1503/jpn.100143 CrossRefGoogle ScholarPubMed
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), 513–520. https://doi.org/10.1080/13554794.2012.701645 CrossRefGoogle Scholar
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), 366–371. https://doi.org/10.1002/mds.10041 CrossRefGoogle ScholarPubMed
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, 188–193. doi:10.1176/appi.neuropsych.17070144CrossRefGoogle ScholarPubMed
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), 1–7. https://doi.org/10.1017/S1355617717001308 Google Scholar
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, 276–292. https://doi.org/10.1016/j.neubiorev.2016.11.020 CrossRefGoogle ScholarPubMed
Levy, R., & Dubois, B. (2006). Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cerebral Cortex, 16, 916–928. https://doi.org/10.1093/cercor/bhj043 CrossRefGoogle ScholarPubMed
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), 1313–1319. https://doi.org/10.1001/archneur.55.10.1313 CrossRefGoogle ScholarPubMed
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, 1–5. https://doi.org/10.4061/2010/930627 CrossRefGoogle ScholarPubMed
Moretti, R., & Signori, R. (2016). Neural correlates for apathy: Frontal-prefrontal and parietal cortical-subcortical circuits. Frontiers in Aging Neuroscience, 8, 289.CrossRefGoogle ScholarPubMed
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. https://doi.org/10.3389/fneur.2014.00073 CrossRefGoogle ScholarPubMed
Njomboro, P., Humphreys, G.W., & Deb, S. (2014). Exploring social cognition in patients with apathy following acquired brain damage. BMC Neurology, 14(1), 18. https://doi.org/10.1186/1471-2377-14-18 CrossRefGoogle ScholarPubMed
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, 69–91. doi:10.1016/B978-0-12-801893-4.00006-7CrossRefGoogle ScholarPubMed
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), 689–692.CrossRefGoogle ScholarPubMed
Pluck, G.C., & Brown, R.G. (2002). Apathy in Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 73(6), 636–642. https://doi.org/10.1136/jnnp.73.6.636 CrossRefGoogle ScholarPubMed
Reitan, R.M. (1955). The relation of the Trail Making Test to organic brain damage. Journal of Consulting Psychology, 19(5), 393–394. https://doi.org/10.1037/h0044509 CrossRefGoogle ScholarPubMed
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), 1153–1158. https://doi.org/10.1136/jnnp-2013-307025 CrossRefGoogle ScholarPubMed
Rolls, E.T. (2000). The orbitofrontal cortex and reward. Cerebral Cortex, 10(3), 284–294. https://doi.org/10.1093/cercor/10.3.284 CrossRefGoogle ScholarPubMed
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), 994–1003. https://doi.org/10.1017/S1355617714000940 CrossRefGoogle ScholarPubMed
Ruff, C.C., & Fehr, E. (2014). The neurobiology of rewards and values in social decision making. Nature Reviews Neuroscience, 15(8), 549–562. https://doi.org/10.1038/nrn3776 CrossRefGoogle ScholarPubMed
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.Google Scholar
Schroeder, U. (2004). Facial expression recognition and subthalamic nucleus stimulation. Journal of Neurology, Neurosurgery, & Psychiatry, 75(4), 648–650. https://doi.org/10.1136/jnnp.2003.019794 CrossRefGoogle ScholarPubMed
Shoulson, I., & Fahn, S. (1979). Huntington disease: Clinical care and evaluation. Neurology, 29(1), 1–3.CrossRefGoogle ScholarPubMed
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, 395–403.CrossRefGoogle ScholarPubMed
Smith, A. (1982). Symbol digit modalities test. Los Angeles, CA: Western Psychological Services.Google Scholar
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), 362–375.CrossRefGoogle Scholar
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), 1–14. https://doi.org/10.1037/a0020937 CrossRefGoogle ScholarPubMed
Stuss, D.T., Van Reekum, R., & Murphy, K.J. (2000). Differentiation of states and causes of apathy. In: The neuropsychology of emotion (pp. 340–363). Retrieved from https://books.google.com/books?hl=en&lr=&id=sBdaUviMAAgC&oi=fnd&pg=PA340&dq=stuss+differentiation+of+states+and+causes+of+apathy&ots=ze4gCrtfXP&sig=SuEQqGcnIfOpYTfeIbiFA35sbmY Google Scholar
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), 791–801. https://doi.org/10.1016/S1474-4422(09)70170-X CrossRefGoogle ScholarPubMed
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, 1411–1418.CrossRefGoogle Scholar
Zigmond, A.S., & Snaith, R.P. (1983). The Hospital Anxiety and Depression Scale. Acta Psychiatrica Scandinavica, 67(6), 361–370. https://doi.org/10.1111/j.1600-0447.1983.tb09716.x CrossRefGoogle ScholarPubMed