Apathy Syndrome in Neurological Diseases – State of the Art and Current Research Directions
Magdalena Roessler-Górecka
Institute of Psychiatry and Neurology in Warsaw, Second Department of Neurologyhttps://orcid.org/0000-0002-1375-5643
Abstract
Aim: Apathy is sometimes indicated as a symptom in various diseases, among others in psychiatry. However, for several decades it has also been distinguished as an independent syndrome accompanying many neurological diseases. Although still omitted from current medical classifications, apathy syndrome is the subject of numerous theoretical and clinical analyses. The spreading of knowledge on it among clinicians – including the possibility of recognizing and differentiating it, especially from depression – is of fundamental importance for the effectiveness of therapeutic interventions. The paper presents definitions and diagnostic criteria of apathy syndrome proposed in the literature. It presents data on its prevalence in various diseases, its relationship with brain pathology, and several clinical variables.
Theses: Contemporary concepts emphasize the syndromic character, multidimensionality of apathy syndrome and links with the broadly understood functions of frontal lobes. The domains of functioning in which symptoms of apathy may be revealed include the cognitive sphere, the emotional sphere, social interactions, and behavior (initiating and maintaining any intentional activity). The relative independence of apathy syndrome from depression is indicated, the importance of apathy syndrome as a prognostic factor for dementia is emphasized, as well as its relationship to quality of life, effectiveness of rehabilitation and psychological burden on caregivers. As for neuronal basis of apathy, a few partially overlapping processes are considered, with significant role of basal ganglia and certain areas of prefrontal cortex.
Conclusion: Dysfunction of any link of complex prefrontal-subcortical circuits may be crucial for occurrence of apathy symptoms, which explains high frequency of this syndrome in brain diseases, especially those with damage to basal ganglia and/or prefrontal cortex. Different severity of symptoms in particular domains and recurrence of abnormality profiles observed depending on the analyzed disease and/or location of brain pathology prompt the search for subtypes of apathy syndrome.
Keywords:
apathy syndrome, basal ganglia, prefrontal cortex, executive dysfunctionsReferences
Abramzon, Y. A., Fratta, P., Traynor, B. J., & Chia, R. (2020). The Overlapping Genetics of Amyotrophic Lateral Sclerosis and Frontotemporal Dementia. Frontiers in Neuroscience, 14, article 42. https://doi.org/10.3389/fnins.2020.00042
Crossref
Google Scholar
Andersson, S., & Bergedalen, A. M. (2002). Cognitive correlates of apathy in traumatic brain injury. Neuropsychiatry, Neuropsychology, & Behavioral Neurology, 15, 184–191. Google Scholar
Andersson, S., Krogstad, J. M., & Finset, A. (1999). Apathy and depressed mood in acquired brain damage: relationship to lesion localization and psychophysiological reactivity. Psychological Medicine, 29, 447–456. https://doi.org/10.1017/s0033291798008046
Crossref
Google Scholar
Ang, Y. S., Lockwood, P., Apps, M. A., Muhammed, K., & Husain, M. (2017). Distinct Subtypes of Apathy Revealed by the Apathy Motivation Index. Plos One, 12(1), https://doi.org/10.1037/t77043-000
Crossref
Google Scholar
Angelelli, P., Paolucci, S., Bivona, U., Piccardi, L., Ciurli, P., Cantagallo, A., Antonucci, G., Fasotti, L., Di Santantonio, A., Grasso, M. G., & Pizzamiglio, L. (2004). Development of neuropsychiatric symptoms in poststroke patients: a cross-sectional study. Acta Psychiatrica Scandinavica, 110(1), 55–63. https://doi.org/10.1111/j.1600-0447.2004.00297.x
Crossref
Google Scholar
Arnould, A., Rochat, L., Azouvi, P., & Van der Linden, M. (2015). Apathetic symptom presentations in patients with severe traumatic brain injury: Assessment, heterogeneity and relationships with psychosocial functioning and caregivers’ burden. Brain Injury, 29(13–14), 1597–1603. https://doi.org/10.3109/02699052.2015.1075156
Crossref
Google Scholar
Baake, V., Coppen, E. M., van Duijn, E., Dumas, E. M., van den Bogaard, S., Scahill, R. I, Johnson, H., Leavitt, B., Durr, A., Tabrizi, S. J., Craufurd, D., & Roos, R. (2018). Apathy and atrophy of subcortical brain structures in Huntington's disease: A two-year follow-up study. NeuroImage: Clinical, 19, 66–70. https://doi.org/doi:10.1016/j.nicl.2018.03.033
Crossref
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, 367–378. https://doi.org/10.1034/j.1600-0404.2001.2000236.x
Crossref
Google Scholar
Bayen, E., Pradat-Diehl, P., Jourdan, C., Ghout, I., Bosserelle, V., Azerad, S., Weiss, J., Joël, M., Aegerter, P., & Azouvi, P. (2013). Predictors of informal care burden 1 year after a severe traumatic brain injury: results from the PariS-TBI study. Journal of Head Trauma Rehabilitation, 28(6), 408–418. https://doi.org/10.1097/htr.0b013e31825413cf
Crossref
Google Scholar
Benoit, M., Clairet, S., Koulibaly, P. M., Darcourt, J., & Robert, P. H. (2004). Brain perfusion correlates of the apathy inventory dimensions of Alzheimer's disease. International Journal of Geriatric Psychiatry, 19(9), 864–869. https://doi.org/10.1002/gps.1163
Crossref
Google Scholar
Bhatia, K. P., & Marsden, C. D. (1994). The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain: A Journal of Neurology, 117(4), 859–876. https://doi.org/10.1093/brain/117.4.859
Crossref
Google Scholar
Bjoerke-Bertheussen, J., Ehrt, U., Rongve, A., Ballard, C., & Aarsland, D. (2012). Neuropsychiatric symptoms in mild dementia with Lewy bodies and Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders, 34(1), 1–6. https://doi.org/10.1159/000339590
Crossref
Google Scholar
Bonnelle, V., Manohar, S., Behrens, T., & Husain, M. (2016). Individual Differences in Premotor Brain Systems Underlie Behavioral Apathy. Cerebral Cortex, 26(2), 807–819. https://doi.org/10.1093/cercor/bhv247
Crossref
Google Scholar
Breitve, M. H., Brønnick, K., Chwiszczuk, L. J., Hynninen, M. J., Aarsland, D., & Rongve, A. (2018). Apathy is associated with faster global cognitive decline and early nursing home admission in dementia with Lewy bodies. Alzheimer's Research & Therapy, 10(1), article 83. https://doi.org/10.1186/s13195-018-0416-5
Crossref
Google Scholar
Brett, C., Sykes, C., & Pires-Yfantouda, R. (2017). Interventions to increase engagement with rehabilitation in adults with acquired brain injury: A systematic review. Neuropsychological Rehabilitation, 27(6), 959–982. https://doi.org/10.1080/09602011.2015.1090459
Crossref
Google Scholar
Brodaty, H., Sachdev, P., Withall, A., Altendorf, A., Valenzuela, M., & Lorentz, L. (2005). Frequency and clinical, neuropsychological and neuroimaging correlates of apathy following stroke – the Sydney Stroke Study. Psychological Medicine, 35(12), 1707–1716. https://doi.org/10.1017/S0033291705006173
Crossref
Google Scholar
Carnes-Vendrell, A., Deus, J., Molina-Seguin, J., Pifarré, J., & Purroy, F. (2019). Depression and Apathy After Transient Ischemic Attack or Minor Stroke: Prevalence, Evolution, and Predictors. Scientific Reports, 9(1), article 16248. https://doi.org/10.1038/s41598-019-52721-5
Crossref
Google Scholar
Carrera, E., & Bogousslavsky, J. (2006). The thalamus and behavior: effects of anatomically distinct strokes. Neurology, 66(12), 1817–1823. https://doi.org/10.1212/01.wnl.0000219679.95223.4c
Crossref
Google Scholar
Cummings, J. L., Mega, M., Gray, K., Rosenberg-Thompson, S., Carusi, D. A., & Gornbein, J. (1994). The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology, 44(12), 2308–2314. https://doi.org/10.1212/WNL.44.12.2308
Crossref
Google Scholar
Da Costa, R., Porto, F., & Marrocos, R. (2013). Dissociation of depression from apathy in traumatic brain injury: a case report. Dementia & Neuropsychologia, 7(3), 312–315. https://doi.org/10.1590/s1980-57642013dn70300014
Crossref
Google Scholar
De Paepe, A., Sierpowska, J., Garcia-Gorro, C., Martinez-Horta, S., Perez-Perez, J., Kulisevsky, J., Rodriguez-Dechicha, N., Vaquer, I., Subira, S., Calopa, M., Muñoz, E., Santacruz, P., Ruiz-Idiago, J., Mareca, C., de Diego-Balaguer, R., & Camara, E. (2019). White matter cortico-striatal tracts predict apathy subtypes in Huntington's disease. Neuroimage: Clinical, 24, article 101965. https://doi.org/10.1016/j.nicl.2019.101965
Crossref
Google Scholar
Derouesné, C., Lacomblez, L., Fiori, N., Gély-Nargeot, M., & Bungener, C. (2012). L'apathie dans la démence frontemporale et la maladie d'Alzheimer: existe-t-il des profils distincts? [Apathy in frontotemporal dementia and Alzheimer's disease: are there distinct profiles?]. Geriatrie et Psychologie Neuropsychiatrie du Vieillissement, 10(1), 107–115. https://doi.org/10.1684/pnv.2012.0315
Crossref
Google Scholar
De Witte, L., Engelborghs, S., Verhoeven, J., De Deyn, P., & Mariën, P. (2008). Disrupted auto-activation, dysexecutive and confabulating syndrome following bilateral thalamic and right putaminal stroke. Behavioural Neurology, 19(3), 145–151. https://dx.doi.org/10.1155/2008/693671
Crossref
Google Scholar
Diehl-Schmid, J., Schmidt, E-M., & Nunnemann, S. (2013). Caregiver burden and needs in frontotemporal dementia. Journal of Geriatric Psychiatry and Neurology, 26(4), 221–229. https://doi.org/10.1177/0891988713498467
Crossref
Google Scholar
D’Iorio, A., Vitale, C., Piscopo, F., Baiano, C., Falanga, A. P., Longo, K., & Santangelo, G. (2017). Impact of anxiety, apathy and reduced functional autonomy on perceived quality of life in Parkinson's disease. Parkinsonism & Related Disorders, 43, 114–117. https://doi.org/10.1016/j.parkreldis.2017.08.003
Crossref
Google Scholar
Douven, E., Kohler, S., & Schievink, S. (2017). Temporal associations between fatigue, depression, and apathy after stroke: results of the cognition and affect after stroke, a prospective evaluation of risks study. Cerebrovascular Diseases, 44, 330–337. https://doi.org/10.1159/000481577
Crossref
Google Scholar
Drevets, W. (1999). Prefrontal cortical-amygdalar metabolism in major depression. Annals of the New York Academy of Sciences, 877, 614–637. https://doi.org/10.1111/j.1749-6632.1999.tb09292.x
Crossref
Google Scholar
Drevets, W., Price, J., Bardgett, M., Reich, T., Todd, R., & Raichle, M. (2002). Glucose metabolism in the amygdala in depression: relationship to diagnostic subtype and plasma cortisol levels. Pharmacology Biochemistry and Behaviour, 71(3), 431–447. https://doi.org/10.1016/S0091-3057(01)00687-6.
Crossref
Google Scholar
Drevets, W., Videen, T., Price, J., Preskorn, S., Carmichael, S., & Raichle, M. (1992). A functional anatomical study of unipolar depression. The Journal of Neuroscience, 12, 3628–3641. https://doi.org/10.1523/JNEUROSCI.12-09-03628.1992
Crossref
Google Scholar
Fernández-Matarrubia, M., Matías-Guiu, J., Cabrera-Martín, M., Moreno-Ramos, T., Valles-Salgado, M., Carreras, J., & Matías-Guiu, J. (2017). Different apathy clinical profile and neural correlates in behavioral variant frontotemporal dementia and Alzheimer's disease. International Journal of Geriatric Psychiatry, 33(1), 141–150. https://doi.org/10.1002/gps.4695
Crossref
Google Scholar
Fisher, C. (1983). Honored guest presentation: abulia minor vs agitated behavior. Clinical Neurosurgery, 31, 9–31. https://doi.org/10.1093/neurosurgery/31.cn_suppl_1.9
Crossref
Google Scholar
Flavell, J., & Nestor, P. (2022). A Systematic Review of Apathy and Depression in Progressive Supranuclear Palsy. Journal of Geriatric Psychiatry and Neurology, 35(3), 280–292. https://doi.org/10.1177/0891988721993545
Crossref
Google Scholar
Giordana, M. T., Ferrero, P., Grifoni, S., Pellerino, A., Naldi, A., & Montuschi, A. (2011). Dementia and cognitive impairment in amyotrophic lateral sclerosis: a review. Neurological Sciences, 32(1), 9–16. https://doi.org/10.1007/s10072-010-0439-6
Crossref
Google Scholar
Guild, E., & Levine, B. (2015). Functional Correlates of Midline Brain Volume Loss in Chronic Traumatic Brain Injury. Journal of the International Neuropsychological Society, 21(8), 650–655. https://doi.org/10.1017/s1355617715000600
Crossref
Google Scholar
Habib, M. (2004). Athymhormia and Disorders of Motivation in Basal Ganglia Disease. The Journal of Neuropsychiatry and Clinical Neurosciences, 16(4), 509–524. https://doi.org/10.1176/JNP.16.4.509
Crossref
Google Scholar
Hama, S., Yamashita, H., Shigenobu, M., Watanabe, A., Hiramoto, K., Kurisu, K., Yamawaki, S., & Kitaoka, T. (2007). Depression or apathy and functional recovery after stroke. International Journal of Geriatric Psychiatry, 22(10), 1046–1051. https://doi.org/10.1002/gps.1866
Crossref
Google Scholar
Ishizaki, J., & Mimura, M. (2011). Dysthymia and apathy: diagnosis and treatment. Depression Research and Treatment, article ID 893905, 1–7. https://doi.org/10.1155/2011/893905
Crossref
Google Scholar
Jaracz, J. (2008). Anatomia depresji w świetle wyników badań neuroobrazowych [The anatomy of depression in light of evidence from neuroimaging studies]. Psychiatria Polska [Polish Psychiatry], 42(6), 875–888. Google Scholar
Jeong, H., Kang, I., Im, J. J., Park, J. S., Na, S. H., Heo, Y., Yang, Y., Chung, Y. A., & Song, I. U. (2018). Brain Perfusion Correlates of Apathy in Alzheimer's Disease. Dementia and Neurocognitive Disorders, 17(2), 50–56. https://doi.org/10.12779/dnd.2018.17.2.50
Crossref
Google Scholar
Jorge, R., Starkstein, S., & Robinson, R. (2010). Apathy following Stroke. The Canadian Journal of Psychiatry, 55(6), 350–354. https://doi.org/10.1177/070674371005500603
Crossref
Google Scholar
Krishnamoorthy, A., & Craufurd, D. (2011). Treatment of Apathy in Huntington’s Disease and Other Movement Disorders. Current Treatment Options in Neurology, 13, 508–519. https://doi.org/10.1007/s11940-011-0140-y
Crossref
Google Scholar
Lanctôt, K. L., Agüera-Ortiz, L., Brodaty, H., Francis, P. T., Geda, Y. E., Ismail, Z., Marshall, G. A., Mortby, M. E., Onyike, C. U., Padala, P. R., Politis, A. M., Rosenberg, P. B., Siegel, E., Sultzer, D. L., & Abraham, E. H. (2017). Apathy associated with neurocognitive disorders: Recent progress and future directions. Alzheimer's & Dementia, 13, 84–100. https://doi.org/10.1016/j.jalz.2016.05.008
Crossref
Google Scholar
Laplane, D., Baulac, M., Widlöcher, D., & Dubois, B. (1984). Pure psychic akinesia with bilateral lesions of basal ganglia. Journal of Neurology, Neurosurgery, and Psychiatry, 47(4), 377–385. https://doi.org/10.1136%2Fjnnp.47.4.377
Crossref
Google Scholar
Lázaro-Perlado, F. (2019). Apathy: A Conceptual Review. Current Psychiatry Research and Reviews, 15, 88–104. http://dx.doi.org/10.2174/1573400515666190306150306
Crossref
Google Scholar
Le Heron, C., Apps, M., & Husain, M. (2018). The anatomy of apathy: A neurocognitive framework for amotivated behaviour. Neuropsychologia, 118(Pt B), 54–67. https://doi.org/10.1016/j.neuropsychologia.2017.07.003
Crossref
Google Scholar
Leśniak, M., Roessler-Górecka, M., Członkowska, A., & Seniów, J. (2022). Clinical significance of self-descriptive apathy assessment in patients with neurological form of Wilson's disease. Neurological Sciences, 43(2), 1385–1394. https://doi.org/10.1007/s10072-021-05366-0
Crossref
Google Scholar
Levy, M. L., Cummings, J. L., Fairbanks, L. A., Masterman, D., Miller, B. L., Craig, A. H., Paulsen, J. S., & Litvan, I. (1998). Apathy is not depression. The Journal of Neuropsychiatry and Clinical Neurosciences, 10(3), 314–319. https://doi.org/10.1176/jnp.10.3.314
Crossref
Google Scholar
Levy, R. (2012). Apathy: a pathology of goal-directed behaviour. A new concept of the clinic and pathophysiology of apathy. Revue Neurologique, 168(8), 585–597. https://doi.org/10.1016/j.neurol.2012.05.003
Crossref
Google Scholar
Levy, R., & Dubois, B. (2006). Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cerebral Cortex, 16(7), 916–928. https://doi.org/10.1093/cercor/bhj043
Crossref
Google Scholar
Lillo, P., Mioshi, E., Zoing, M., Kiernan, M., & Hodges, J. (2011). How common are behavioural changes in amyotrophic lateral sclerosis? Amyotrophic Lateral Sclerosis, 12(1), 45–51. https://doi.org/10.3109/17482968.2011.639376
Crossref
Google Scholar
Litvan, I., Mega, M., Cummings, J., & Fairbanks, L. (1996). Neuropsychiatric aspects of progressive supranuclear palsy. Neurology, 47, 1184–1189. https://doi.org/10.1212/WNL.47.5.1184
Crossref
Google Scholar
Ma, L. (2020). Depression, anxiety, and apathy in mild cognitive impairment: Current perspectives. Frontiers in Aging Neuroscience, 12, article 9. https://doi.org/10.3389/fnagi.2020.00009
Crossref
Google Scholar
Madhusoodanan, S., Ting, M., Farah, T., & Ugur, U. (2015). Psychiatric aspects of brain tumors: A review. World Journal of Psychiatry, 5(3), 273–285. https://doi.org/10.5498/wjp.v5.i3.273
Crossref
Google Scholar
Marin, R. (1990). Differential diagnosis and classification of apathy. American Journal of Psychiatry, 147(1), 22–30. https://doi.org/10.1176/ajp.147.1.22
Crossref
Google Scholar
Marin, R. (1991). Apathy: a neuropsychiatric syndrome. The Journal of Neuropsychiatry and Clinical Neurosciences, 3(3), 243–254. https://doi.org/10.1176/jnp.3.3.243
Crossref
Google Scholar
Marin, R., & Wilkosz, P. (2005). Disorders of diminished motivation. The Journal of Head Trauma Rehabilitation, 20(4), 377–388. https://doi.org/10.1097/00001199-200507000-00009
Crossref
Google Scholar
Marin, R. S., Biedrzycki, R. C., & Firinciogullari, S. (1991). Reliability and validity of the Apathy Evaluation Scale. Psychiatry Research, 38(2), 143–162. https://doi.org/10.1016/0165-1781(91)90040-v
Crossref
Google Scholar
McFarland, B., & Klein, D. (2009). Emotional reactivity in depression: diminished responsiveness to anticipated reward but not to anticipated punishment or to nonreward or avoidance. Depression and Anxiety, 26(2), 117–122. https://doi.org/10.1002/da.20513
Crossref
Google Scholar
Mele, B., Van, S., Holroyd-Leduc, J., Ismail, Z., Pringsheim, T., & Goodarzi, Z. (2020). Diagnosis, treatment and management of apathy in Parkinson's disease: a scoping review. BMJ Open, 10(9), https://doi.org/10.1136/bmjopen-2020-037632
Crossref
Google Scholar
Merrilees, J., Dowling, G., Hubbard, E., Mastick, J., Ketelle, R., & Miller, B. (2013). Characterization of apathy in persons with frontotemporal dementia and the impact on family caregivers. Alzheimer Disease and Associated Disorders, 27(1), 62–67. https://doi.org/10.1097/wad.0b013e3182471c54
Crossref
Google Scholar
Millar, D., Griffiths, P., Zermansky, A., & Burn, D. (2006). Characterizing behavioral and cognitive dysexecutive changes in progressive supranuclear palsy. Movement Disorders, 21(2), 199–207. https://doi.org/10.1002/mds.20707
Crossref
Google Scholar
Miller, D. S., Robert, P., Ereshefsky, L., Adler, L., Bateman, D., Cummings, J., DeKosky, S. T., Fischer, C. E., Husain, M., Ismail, Z., Jaeger, J., Lerner, A. J., Li, A., Lyketsos, C. G., Manera, V., Mintzer, J., Moebius, H. J., Mortby, M., Meulien, D., … Lanctôt, K. L. (2021). Diagnostic criteria for apathy in neurocognitive disorders. Alzheimer's & Dementia: The Journal of the Alzheimer's Association, 17(12), 1892–1904. https://doi.org/10.1002/alz.12358
Crossref
Google Scholar
Monsalve, C., B., Guitart, B. M., López, R., Vilasar, B. A., & Quemada, J. (2012). Perfil psicopatológico de pacientes con traumatismo craneoencefálico evaluados mediante el Inventario Neuropsiquiátrico [Psychopatological evaluation of traumatic brain injury patients with the Neuropsychiatric Inventory]. Revista de Psiquiatria y Salud Mental, 5(3), 160–166.
Crossref
Google Scholar
Motomura, K., Kawamura, A., Ohka, F., Aoki, K., Nishikawa, T., Yamaguchi, J., Kibe, Y., Shimizu, H., Maeda, S., & Saito, R. (2023). Predictive factors of post-operative apathy in patients with diffuse frontal gliomas undergoing awake brain mapping. Journal of Neuropsychology, 18(S1), 73–84. https://doi.org/10.1111/jnp.12345
Crossref
Google Scholar
Naarding, P., Janzing, J., Eling, P., van der Werf, S., & Kremer, B. (2009). Apathy is not depression in Huntington’s disease. The Journal of Neuropsychiatry and Clinical Neurosciences, 21, 266–270. https://doi.org/10.1176/jnp.2009.21.3.266
Crossref
Google Scholar
Nobis, L., & Husain, M. (2018). Apathy in Alzheimer's disease. Current Opinion in Behavioral Sciences, 22, 7–13. https://doi.org/10.1016/j.cobeha.2017.12.007
Crossref
Google Scholar
Pachi, I., Koros, C., Simitsi, A., Papadimitriou, D., Bougea, A., Prentakis, A., Papagiannakis, N., Bozi, M., Antonelou, R., Angelopoulou, E., Beratis, I., Stamelou, M., Trapali, X., Papageorgiou, S., & Stefanis, L. (2021). Apathy: An underestimated feature in GBA and LRRK2 non-manifesting mutation carriers. Parkinsonism and Related Disorders, 91, 1–8. https://doi.org/10.1016/j.parkreldis.2021.08.008
Crossref
Google Scholar
Pagonabarraga, J., Kulisevsky, J., Strafella, A., & Krack, P. (2015). Apathy in Parkinson's disease: clinical features, neural substrates, diagnosis, and treatment. The Lancet Neurology, 14(5), 518–531. https://doi.org/10.1016/s1474-4422(15)00019-8
Crossref
Google Scholar
Peng, Y., Shao, Ch., Gong, Y., Wu, X., Tang, W., & Shi, S. (2015). Relationship between apathy and tumor location, size, and brain edema in patients with intracranial meningioma, Neuropsychiatric Disease and Treatment, 11, 1685–1693. https://doi.org/10.2147/ndt.s85288
Crossref
Google Scholar
Pluck, G., & Brown, R. (2002). Apathy in Parkinson’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 73, 636–642. https://doi.org/10.1136/jnnp.73.6.636
Crossref
Google Scholar
Pont-Sunyer, C., Hotter, A., Gaig, C., Seppi, K., Compta, Y., Katzenschlager, R., Mas, N., Hofeneder, D., Brücke, T., Bayés, A., Wenzel, K., Infante, J., Zach, H., Pirker, W., Posada, I. J., Álvarez, R., Ispierto, L., De Fàbregues, O., Callén, A., … Tolosa, E. (2015). The Onset of Nonmotor Symptoms in Parkinson's disease (The ONSET PD Study). Movement Disorders, 30, 229–237. https://doi.org/10.1002/mds.26077
Crossref
Google Scholar
Radakovic, R., & Abrahams, S. (2014). Developing a new apathy measurement scale: Dimensional Apathy Scale. Psychiatry Research, 219(3), 658–663. https://doi.org/10.1016/j.psychres.2014.06.010
Crossref
Google Scholar
Radakovic, R., Davenport, R., Starr, J., & Abrahams, S. (2018). Apathy dimensions in Parkinson's disease. International Journal of Geriatric Psychiatry, 33(1), 151–158. https://doi.org/10.1002/gps.4697
Crossref
Google Scholar
Radakovic, R., Stephenson, L., Colville, S., Swingler, R., Chandran, S., & Abrahams, S. (2016). Multidimensional apathy in ALS: validation of the Dimensional Apathy Scale. Journal of Neurology, Neurosurgery & Psychiatry, 87(6), 663–669.
Crossref
Google Scholar
Radakovic, R., Stephenson, L., Newton, J., Crockford, C., Swingler, R., Chandran, S., & Abrahams, S. (2017). Multidimensional Apathy and Executive Dysfunction in Amyotrophic Lateral Sclerosis. Cortex, 94, 142–151. https://doi.org/10.1016/j.cortex.2017.06.023
Crossref
Google Scholar
Ready, R., Mathews, M., Leserman, A., & Paulsen, J. (2008). Patient and caregiver quality of life in Huntington's disease. Movement Disorders, 23(5), 721–726. https://doi.org/10.1002/mds.21920
Crossref
Google Scholar
Robert, P., Lanctôt, K., Agüera-Ortiz, L., Aalten, P., Bremond, F., Defrancesco, M., Hanon, C., David, R., Dubois, B., Dujardin, K., Husain, M., König, A., Levy, R., Mantua, V., Meulien, D., Miller, D., Moebius, H., Rasmussen, J., Robert, G., … Manera, V. (2018). Is it time to revise the diagnostic criteria for apathy in brain disorders? The 2018 international consensus group. European Psychiatry, 54, 71–76. https://doi.org/10.1016/j.eurpsy.2018.07.008
Crossref
Google Scholar
Robert, P., Onyike, C. U., Leentjens, A. F., Dujardin, K., Aalten, P., Starkstein, S., Verhey, F. R., Yessavage, J., Clement, J. P., Drapier, D., Bayle, F., Benoit, M., Boyer, P., Lorca, P. M., Thibaut, F., Gauthier, S., Grossberg, G., Vellas, B., & Byrne, J. (2009). Proposed diagnostic criteria for apathy in Alzheimer's disease and other neuropsychiatric disorders. European Psychiatry, 24(2), 98–104. https://doi.org/10.1016/j.eurpsy.2008.09.001
Crossref
Google Scholar
Santa, N., Sugimori, H., Kusuda, K., Yamashita, Y., Ibayashi, S., & Iida, M. (2008). Apathy and functional recovery following first-ever stroke. International Journal of Rehabilitation Research, 31(4), 321–326. https://doi.org/10.1097/MRR.0b013e3282fc0f0e
Crossref
Google Scholar
Seniów, J., Komajda, R., & Zaborski, J. (2005). Zespół apatii w konsekwencji uszkodzenia mózgu – trudny problem neurorehabilitacji [Apathy syndrome as a consequence of brain injury – a difficult problem in neurorehabilitation]. Rehabilitacja Medyczna [Medical Rehabilitation], 9(2), 15–19. Google Scholar
Sockeel, P., Dujardin, K., Devos, D., Denève, C., Destée, A., & Defebvre, L. (2006). The Lille apathy rating scale (LARS), a new instrument for detecting and quantifying apathy: validation in Parkinson’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 77(5), 579–584. https://doi.org/10.1136/jnnp.2005.075929
Crossref
Google Scholar
Stanton, B., Leigh, P., Howard, R., Barker, G., & Brown, R. (2013). Behavioural and emotional symptoms of apathy are associated with distinct patterns of brain atrophy in neurodegenerative disorders. Journal of Neurology, 260(10), 2481–2490. https://doi.org/10.1007/s00415-013-6989-9
Crossref
Google Scholar
Starkstein, S., Fedoroff, J., Price, T., Leiguarda, R., & Robinson, R. (1993). Apathy following cerebrovascular lesions. Stroke, 24(11), 1625–1630. https://doi.org/10.1161/01.str.24.11.1625
Crossref
Google Scholar
Starkstein, S., & Manes, F. (2000). Apathy and depression following stroke. CNS Spectrums, 5(3), 43–50. https://doi.org/10.1017/s1092852900012955
Crossref
Google Scholar
Starkstein, S., Mayberg, H., Preziosi, T., Andrezejewski, P., Leiguarda, R., & Robinson, R. (1992). Reliability, validity, and clinical correlates of apathy in Parkinsons disease. Journal of Neuropsychiatry and Clinical Neurosciences, 4(2), 134–139. https://doi.org/10.1176/jnp.4.2.134
Crossref
Google Scholar
Starkstein, S., Merello, M., Jorge, R., Brockman, S., Bruce, D., & Power, B. (2009). The syndromal validity and nosological position of apathy in Parkinson's disease. Movement Disorders, 24(8), 1211–1216. https://doi.org/10.1002/mds.22577
Crossref
Google Scholar
Starkstein, S., & Pahissa, J. (2014). Apathy following traumatic brain injury. The Psychiatric clinics of North America, 37(1), 103–112. https://doi.org/10.1016/j.psc.2013.10.002
Crossref
Google Scholar
Starkstein, S., Petracca, G., Chemerinski, E., & Kremer, J. (2001). Syndromic validity of apathy in Alzheimer’s disease. The American Journal of Psychiatry, 158(6), 872–877. https://doi.org/10.1176/appi.ajp.158.6.872
Crossref
Google Scholar
Steffens, D. C., Fahed, M., Manning, K. J., & Wang, L. (2022). The neurobiology of apathy in depression and neurocognitive impairment in older adults: a review of epidemiological, clinical, neuropsychological and biological research. Translational Psychiatry, 12(1), https://doi.org/10.1038/s41398-022-02292-3
Crossref
Google Scholar
Stuss, D. (2011). Functions of the frontal lobes: relation to executive functions. Journal of the International Neuropsychological Society, 17(5), 759–765. https://psycnet.apa.org/doi/10.1017/S1355617711000695
Crossref
Google Scholar
Stuss, D., & Benson, F. (1986). The Frontal Lobes. Raven Press. Google Scholar
Stuss, D., van Reekum, R., & Murphy, K. (2000). Differentiaton of states and causes of apathy. In J. Borod (Ed.), The neuropsychology of emotion (pp. 340–352). Oxford University Press. Google Scholar
Tay, J., Morris, R., & Markus, H. (2021). Apathy after stroke: Diagnosis, mechanisms, consequences, and treatment. International Journal of Stroke, 16(5), 510–518. https://doi.org/10.1177/1747493021990906
Crossref
Google Scholar
Tay, J., Morris, R., Tuladhar, A., Husain, M., de Leeuw, F., & Markus, H. (2020). Apathy, but not depression, predicts all-cause dementia in cerebral small vessel disease. Journal of Neurology, Neurosurgery & Psychiatry, 91(9), 953–959. https://doi.org/10.1136/jnnp-2020-323092
Crossref
Google Scholar
Theleritis, C. (2017). Pharmacological and Nonpharmacological Treatment for Apathy in Alzheimer Disease: A systematic review across modalities. The Journal of Geriatric Psychiatry and Neurology, 30(1), 26–49. https://doi.org/10.1177/0891988716678684
Crossref
Google Scholar
Thompson, J., Harris, J., & Sollom, A. (2012). Longitudinal evaluation of neuropsychiatric symptoms in Huntington’s disease. Journal of Neuropsychiatry and Clinical Neurosciences, 24, 53–60. https://doi.org/10.1176/appi.neuropsych.11030057
Crossref
Google Scholar
Zarandy, J., Yoon, S., Saravanan, S., Das, S., & Thomas, S. (2023). Differential Diagnostic Considerations in a Patient With New Onset Apathy: A Case Study on Frontal Lobe Glioblastoma Multiforme. The Journal of Integrated Primary Care, 1(1), article 3. https://digitalcommons.pcom.edu/jipc/vol1/iss1/3 Google Scholar
Zoon, T., van Rooijen, G., Balm, G., Bergfeld, I., Daams, J., Krack, P., Denys, D., & de Bie, R. (2021). Apathy Induced by Subthalamic Nucleus Deep Brain Stimulation in Parkinson's Disease: A Meta-Analysis. Movement Disorders, 36(2), 317–326. https://doi.org/10.1002/mds.28390
Crossref
Google Scholar
Institute of Psychiatry and Neurology in Warsaw, Second Department of Neurology
https://orcid.org/0000-0002-1375-5643
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