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Neural correlates of apathy in patients with neurodegenerative disorders, acquired brain injury, and psychiatric disorders
Open accessAbstract
Apathy can be described as a loss of goal-directed purposeful behavior and is common in a variety of neurological and psychiatric disorders. Although previous studies investigated associations between abnormal brain functioning and apathy, it is unclear whether the neural basis of apathy is similar across different pathological conditions. The purpose of this systematic review was to provide an extensive overview of the neuroimaging literature on apathy including studies of various patient populations, and evaluate whether the current state of affairs suggest disorder specific or shared neural correlates of apathy. Results suggest that abnormalities within fronto-striatal circuits are most consistently associated with apathy across the different pathological conditions. Of note, abnormalities within the inferior parietal cortex were also linked to apathy, a region previously not included in neuroanatomical models of apathy. The variance in brain regions implicated in apathy may suggest that different routes towards apathy are possible. Future research should investigate possible alterations in different processes underlying goal-directed behavior, ranging from intention and goal-selection to action planning and execution.
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“Concerning apathy, it is the case that limbic-frontal-subcortical circuits are frequently implicated in the pathophysiology of this condition in clinical populations (van Reekum et al., 2005; Kos et al., 2016).”
From The cingulum bundle: Anatomy, function, and dysfunction (2018) · cites this paper as Kos et al., 2016
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Post-Stroke Neuropsychiatric Complications: Types, Pathogenesis, and Therapeutic Intervention
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Apathy in schizophrenia: A review of neuropsychological and neuroanatomical studies
Bortolon, C., Macgregor, A., Capdevielle, D., & Raffard, S. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.09.033 · Cited by 69
Apathy as a Treatment Target in Alzheimer's Disease: Implications for Clinical Trials
Mortby, M. E., Adler, L., Agüera-Ortíz, L., Bateman, D. R., Brodaty, H., Cantillon, M., Geda, Y. E., Ismail, Z., Lanctôt, K. L., Marshall, G. A., et al. (2021) · American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2021.06.016 · Cited by 69
Apathy in Parkinson’s Disease: Clinical Patterns and Neurobiological Basis
Béreau, M., Waes, V. V., Servant, M., Magnin, É., Tatu, L., & Anheim, M. (2023) · Cells · doi:10.3390/cells12121599 · Cited by 66
“In recent years, structural and functional neuroimaging studies carried out in PD, other neurodegenerative disease and stroke patients have improved the understanding of the anatomical correlates of apathy [87,88].”
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Dysfunctional effort-based decision-making underlies apathy in genetic cerebral small vessel disease
Heron, C. J. L., Manohar, S., Plant, O., Muhammed, K., Griffanti, L., Nemeth, A. H., Douaud, G., Markus, H. S., & Husain, M. (2018) · Brain · doi:10.1093/brain/awy257 · Cited by 45
“, 2017), are the same regions that have been associated with apathy in neuroimaging studies across different modalities and neurological conditions (Kos et al., 2016; Le Heron et al., 2017).”
The neuroimaging basis of apathy: Empirical findings and conceptual challenges
STARKSTEIN, S. E., & Brockman, S. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.01.042 · Cited by 42
“Kos and co-workers’ review (Kos et al., 2016) included 14 studies using MRI and 4 studies using (18)Fluoro-deoxy-glucose (FDG) PET.”
Neuropsychiatric symptoms in spinocerebellar ataxias and Friedreich ataxia
Karamazovová, S., Matušková, V., Ismail, Z., & Vyhnálek, M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105205 · Cited by 45
“associated with lower activity and metabolism in the cerebellum and the development of apathy has been reported in patients following an isolated cerebellar stroke (Kos et al., 2016; Le Heron et al., 2018).”
BackgroundStepien, M., Manoliu, A., Kubli, R., Schneider, K., Tobler, P. N., Seifritz, E., Herdener, M., Kaiser, S., & Kirschner, M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0198215 · Cited by 45
Lateral parietal cortex in the generation of behavior: Implications for apathy
Tumati, S., Martens, S., de Jong, B. M., & Aleman, A. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.12.003 · Cited by 40
“In imaging studies across disorders, apathy is associated with deficits in multiple brain regions (Kos et al., 2016), with the most common region being the dorsal anterior cingulate cortex (dACC) (McIntosh”
InfluentialSelf-citationKirschner, M., Schmidt, A., Hodzic-Santor, B. H., Burrer, A., Manoliu, A., Zeighami, Y., Yau, Y. H. C., Abbasi, N., Maatz, A., Habermeyer, B., et al. (2020) · Schizophrenia Bulletin · doi:10.1093/schbul/sbaa169 · Cited by 40
van der Stouwe, E. C. D., van Busschbach, J. T., de Vries, B., Cahn, W., Aleman, A., & Pijnenborg, G. H. M. (2018) · NeuroImage Clinical · doi:10.1016/j.nicl.2018.04.018 · Cited by 43
“With regard to negative symptoms such as apathy, future research should investigate the effect on the fronto-subcortical circuitry and the anterior cingulate cortex (ACC) and the inferior parietal cortex as regions of interest (Kos et al., 2016).”
Self-citationJones, S. A., De Marco, M., Manca, R., Bell, S. M., Blackburn, D. J., Wilkinson, I. D., Soininen, H., & Venneri, A. (2019) · Cortex · doi:10.1016/j.cortex.2019.04.008 · Cited by 37
“Particularly, the anterior cingulate cortex (ACC), the prefrontal cortex, and sub-cortical regions such as amygdala, thalamus and basal ganglia have been reported as the 1 LIST OF ABBREVIATIONSぎ ACCぎ ;ﾐデWヴｷﾗヴ Iｷﾐｪ┌ﾉ;デW IﾗヴデW┝き ADぎ Aﾉ┣ｴWｷﾏWヴげゲ SｷゲW;ゲWき DLPFC: dorsolateral prefrontal cortex; MCI: Mild cognitive impairme…”
BackgroundRaimo, S., Santangelo, G., D’Iorio, A., Trojano, L., & Grossi, D. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9959-0 · Cited by 37
“As stated above, the inferior frontal gyrus would be associated to the ability to generate and maintain purposeful behaviors (Levy and Dubois 2006), whereas the right inferior parietal cortex would have a key role in intentional movements and movement awareness (Kos et al. 2016, 2017).”
BackgroundInfluentialNetwork neuroscience of apathy in cerebrovascular disease
Tay, J., Lisiecka, D. M., Hollocks, M. J., Tuladhar, A. M., Barrick, T. R., Förster, A., O'Sullivan, M. J., Husain, M., de Leeuw, F., Morris, R. G., et al. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101785 · Cited by 39
“late cortex (ACC), medial orbitofrontal cortex (OFC), ventral striatum, medial thalamus, and ventral tegmental area (Kos et al., 2016; Le Heron et al., 2018a).”
BackgroundFrom apathy to addiction: Insights from neurology and psychiatry
Kirschner, M., Rabinowitz, A. G., Singer, N., & Dagher, A. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109926 · Cited by 37
Functional network topology associated with apathy in Alzheimer's disease
Tumati, S., Marsman, J.-B. C., Deyn, P. P. D., Martens, S., & Aleman, A. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.01.158 · Cited by 31
“As noted above, apathy in MCI and AD patients was not only associated with fronto-subcortical circuits but also with broader regions of the association cortex (Kos et al., 2016; Stella et al., 2014; Fig.”
Self-citationCommon neural deficits across reward functions in major depression: a meta-analysis of fMRI studies
Zhao, X., Wu, S., Li, X., Liu, Z., Lu, W., Lin, K., & Shao, R. (2024) · Psychological Medicine · doi:10.1017/s0033291724001235 · Cited by 29
Berthier, M. L., Edelkraut, L., López‐González, F. J., López-Barroso, D., Mohr, B., Friedemann Pulvermüller, A., STARKSTEIN, S. E., Jorge, R. E., Torres‐Prioris, M. J., & Dávila, G. (2022) · Brain and Language · doi:10.1016/j.bandl.2022.105205 · Cited by 27
“Post-stroke apathy and depression are clinically dissociable and result from disruptions of different subcomponents of networks regulating motivated behavior and mood (Jorge et al., 2010; Kos et al., 2016; Le Heron et al., 2018; Riva-Posse et al., 2019; Starkstein & Brockman, 2018).”
Apathy is Associated with Critical Psychological Determinants of Medication Adherence in HIV Disease
Babicz, M. A., Woods, S. P., Fazeli, P. L., & Morgan, E. E. (2020) · Journal of Clinical Psychology in Medical Settings · doi:10.1007/s10880-020-09715-7 · Cited by 26
Brakowski, J., Manoliu, A., Homan, P., Bosch, O. G., Herdener, M., Seifritz, E., Kaiser, S., & Kirschner, M. (2020) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2020.10.047 · Cited by 29
Apathy and brain alterations in Parkinson's disease: a multimodal imaging study
Lucas-Jiménez, O., Ojeda, N., Peña, J., Cabrera-Zubizarreta, A., Díez-Cirarda, M., Gómez-Esteban, J., Gómez-Beldarrain, M., & Ibarretxe-Bilbao, N. (2018) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.578 · Cited by 25
“It is potentially interesting that in line with resting-state FC results, hyperconnectivity differences have been found in other pathologies, and that hyperconnectivity has been related to apathy symptoms.(41) Specifically, some studies reported increased FC in bipolar and schizophrenia patients involving frontal and…”
ResultWen, M.-C., Thiéry, A. H., Tseng, W.-Y. I., Kok, T., Xu, Z., Chua, S. T., & Tan, L. C. S. (2020) · Psychological Medicine · doi:10.1017/s0033291720001907 · Cited by 24
“, 2019) and may represent the common neural substrates of apathy across varied neurological disorders (Kos et al., 2016; Moretti & Signori, 2016; Raimo et al., 2019).”
BackgroundSetiadi, T. M., Martens, S., Opmeer, E. M., Marsman, J.-B. C., Tumati, S., Reesink, F. E., Deyn, P. P. D., Aleman, A., & Ćurĉić‐Blake, B. (2021) · NeuroImage Clinical · doi:10.1016/j.nicl.2021.102567 · Cited by 24
Self-citationApathy is associated with parietal cortical-subcortical dysfunction in ALS.
Caga, J., Tu, S.-C., Dharmadasa, T., Tse, N. Y., Zoing, M. C., Huynh, W., Mahoney, C. J., Ahmed, R., & Kiernan, M. (2021) · Cortex; a journal devoted to the study of the nervous system and behavior · doi:10.1016/j.cortex.2021.02.029 · Cited by 23
Lower Choline and Myo-Inositol in Temporo-Parietal Cortex Is Associated With Apathy in Amnestic MCI
Tumati, S., Opmeer, E. M., Marsman, J.-B. C., Martens, S., Reesink, F. E., Deyn, P. P. D., & Aleman, A. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00106 · Cited by 24
“…may be present in the various regions implicated in apathy – the DACC and TPC, which were empirically associated with apathy (Stella et al., 2014; Kos et al., 2016); the DLPFC, as suggested by theoretical models of apathy (Levy and Dubois, 2006); and the PCC, where Abbreviations: 1 H-MRS,…”
BackgroundMethodSelf-citationCosta, A., Peppe, A., Zabberoni, S., Scalici, F., Caltagirone, C., & Carlesimo, G. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.05.016 · Cited by 22
Perri, R., Turchetta, C. S., Caruso, G., Fadda, L., Caltagirone, C., & Carlesimo, G. A. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.01.039 · Cited by 22
“However, neuroimaging studies have also documented an association between apathy and damage to the anterior cingulate, orbitofrontal, medial frontal and insular cortex in AD (Kos et al., 2016); all of these regions are involved in sensory and emotional information processing and affective modulation (Levy and Dubois,…”
InfluentialApathy Is Related to Cognitive Control and Striatum Volumes in Prodromal Huntington’s Disease
Misiura, M. B., Ciarochi, J., Vaidya, J. G., Bockholt, J. H., Johnson, H. J., Calhoun, V. D., Paulsen, J. S., Turner, J. A., & the PREDICT-HD Investigators and Working Group (2019) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617719000067 · Cited by 21
“Levy and Czernecki (2006) define apathy as a reduction of voluntary, goal-directed behaviors.”
BackgroundSun, H.-H., Pan, P., Hu, J.-B., Chen, J., Wang, X.-Y., & Liu, C.-F. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.05.145 · Cited by 20
Brain gray matter abnormalities in progressive supranuclear palsy revisited
Pan, P.-L., Liu, Y., Zhang, Y., Zhao, H., Ye, X., & Xu, Y. (2017) · OncoTarget · doi:10.18632/oncotarget.20895 · Cited by 16
“The ACC is engaged in the medial frontal-subcortical circuit and in the dorsolateral prefrontal-subcortical circuit, dysfunction of which are responsible for apathy and executive dysfunction, respectively [57-59, 74, 75].”
BackgroundStructural Brain Differences Between Cognitively Impaired Patients With and Without Apathy
Chan, N. K., Gerretsen, P., Chakravarty, M. M., Blumberger, D. M., Caravaggio, F., Brown, E. E., & Graff‐Guerrero, A. (2020) · American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2020.12.008 · Cited by 19
Basavaraju, R., Feng, X., France, J., Huey, E. D., & Provenzano, F. A. (2020) · Journal of Geriatric Psychiatry and Neurology · doi:10.1177/0891988720964258 · Cited by 18
“Previous studies on the neural correlates of apathy(12,13) in FTD have implicated different parts of the frontal lobes including the dorsolateral prefrontal cortex (DLPFC),(27-29) ventromedial superior frontal gyrus,(30) anterior cingulate cortex (ACC)(27,29) and orbitofrontal cortex (OFC), 30 predominantly on the rig…”
Gray Matter Vulnerabilities Predict Longitudinal Development of Apathy in Huntington's Disease
Paepe, A. E. D., Ara, A., García-Gorro, C., Martínez-Horta, S., Pèrez-Pèrez, J., Kulisevsky, J., Rodríguez-Dechicha, N., Vaquer, I., Subirà, S., Calopa, M., et al. (2021) · Movement Disorders · doi:10.1002/mds.28638 · Cited by 14
“All in all, the MCC (BA24) has been associated with apathy severity in both healthy and neurologically impaired populations.(46,49,55) For example, apathy in otherwise healthy individuals has been related with decreased salience-related processing in ACC(56) as well as a greater recruitment of ACC and supplementary mo…”
BackgroundBehavioural changes in frontotemporal dementia and their cognitive and neuroanatomical correlates
Rouse, M., Husain, M., Garrard, P., Patterson, K., Rowe, J., & Ralph, M. L. (2024) · medRxiv · doi:10.1093/brain/awaf061 · Cited by 15
“Atrophy or hypometabolism in the anterior cingulate cortex has been linked strongly with apathy in FTD 99-102 and in other neurodegenerative disorders, such as Alzheimer’s disease 103,104 and Parkinson’s disease.”
Servaas, M. N., Kos, C., Gravel, N., Renken, R. J., Marsman, J.-B. C., van Tol, M., & Aleman, A. (2018) · Schizophrenia Bulletin · doi:10.1093/schbul/sby108 · Cited by 15
Self-citationStrengths and Weaknesses of the Vascular Apathy Hypothesis: A Narrative Review
Wouts, L., Marijnissen, R. M., Voshaar, R. C. O., & Beekman, A. T. F. (2022) · American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2022.09.016 · Cited by 18
Apathy in Patients With Cerebral Amyloid Angiopathy
Chokesuwattanaskul, A., Zotin, M. C. Z., Schoemaker, D., Sveikata, L., Gurol, M. E., Greenberg, S. M., & Viswanathan, A. (2023) · Neurology · doi:10.1212/wnl.0000000000207200 · Cited by 16
“Indeed, studies in neurodegenerative diseases and SVDs have confirmed the association of the integrity of the forceps minor and other parts of the corpus callosum with apathy.(5,11,12,42,43)”
BackgroundYan, H., Wu, H., Cai, Z., Du, S., Li, L., Xu, B., Chang, C., & Wang, N. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1181558 · Cited by 17
Moretti, R., Caruso, P., & Ben, M. D. (2017) · Parkinson s Disease · doi:10.1155/2017/6219851 · Cited by 17
“, [34] an inverse correlation between catecholaminergic binding potential, indicative of a specific combined loss of dopamine and noradrenaline innervation, and apathy was found in the bilateral ventral striatum in an exploratory resting-state analysis in PD [38].”
Apathy is related to reduced activation in cognitive control regions during set‐shifting
Klaasen, N. G., Kos, C., Aleman, A., & Opmeer, E. M. (2017) · Human Brain Mapping · doi:10.1002/hbm.23556 · Cited by 15
“For the apathy mask, a map was used including brain areas related to apathy in various disorders [Kos et al., 2016].”
MethodSelf-citationNeural basis of self-initiative in relation to apathy in a student sample
Kos, C., Klaasen, N. G., Marsman, J.-B. C., Opmeer, E. M., Knegtering, H., Aleman, A., & van Tol, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-03564-5 · Cited by 14
Self-citationCaravaggio, F., Fervaha, G., Iwata, Y., Plitman, E., Chung, J., Nakajima, S., Mar, W., Gerretsen, P., Kim, J., Chakravarty, M., et al. (2017) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.4818 · Cited by 13
Spirituality as a Therapeutic Approach for Severe Mental Illness: Insights from Neural Networks
Knegtering, H., Bruggeman, R., & Spoelstra, S. K. (2024) · Religions · doi:10.3390/rel15040489 · Cited by 19
Self-citationResting-State Functional Connectivity Signatures of Apathy in Community-Living Older Adults
Jang, J. Y., Han, S. D., Yew, B., Blanken, A. E., Dutt, S., Li, Y., Ho, J. K., Gaubert, A., & Nation, D. A. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.691710 · Cited by 12
“Reviews integrating structural and functional correlates of apathy across different disorders have identified regions commonly associated with apathy, including the anterior cingulate cortex (ACC), ventral striatum (nucleus accumbens; NAcc), thalamus, orbitofrontal cortex (OFC), and insula (IC) (Kos et al., 2016; Le H…”
BackgroundThe neural correlates of apathy in schizophrenia: An exploratory investigation
Caravaggio, F., Fervaha, G., Menon, M., Remington, G., Graff-Guerrero, A., & Gerretsen, P. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.10.027 · Cited by 11
“These include the dorsolateral prefrontal cortex (DLPFC), anterior cingulate cortex (ACC), inferior parietal cortex, and the ventral striatum (VS) (Kos et al., 2016; Sallet et al., 2011).”
The Neural Correlates of Negative Symptoms in Schizophrenia: Examples From MRI Literature
Mørch-Johnsen, L. E., Agartz, I., & Jensen, J. (2017) · Clinical EEG and Neuroscience · doi:10.1177/1550059417746214 · Cited by 12
Cortical Thickness in Alcohol Dependent Patients With Apathy
Yang, K., Yang, Q., Niu, Y., Fan, F., Chen, S., Luο, X., Tan, S., Wang, Z., Tong, J., Yang, F., et al. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00364 · Cited by 12
“In imaging studies of various brain disorders, apathy has been associated with structural and function deficits of multiple brain regions (17), particularly the dorsal anterior cingulate cortex (dACC) (18).”
BackgroundPlanning in amnestic mild cognitive impairment: an fMRI study
Lejko, N., Tumati, S., Opmeer, E. M., Marsman, J.-B. C., Reesink, F. E., Deyn, P. P. D., Aleman, A., & Ćurĉić‐Blake, B. (2021) · Experimental Gerontology · doi:10.1016/j.exger.2021.111673 · Cited by 12
“…Alzheimer's disease (AD), apathy has been associated with structural abnormalities in frontal brain areas, including the anterior cingulate cortex, the orbitofrontal cortex, and the dorsolateral prefrontal cortex (Kos et al., 2016; Raimo et al., 2019; Stella et al., 2014; Theleritis et al., 2014).”
BackgroundSelf-citationApathy is not associated with reduced ventral striatal volume in patients with schizophrenia
Burrer, A., Caravaggio, F., Manoliu, A., Plitman, E., Guetter, K., Habermeyer, B., Stämpfli, P., Abivardi, A., Schmidt, A., Borgwardt, S., et al. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2020.08.018 · Cited by 12
White matter microstructural associates of apathy-avolition in schizophrenia
Abdolalizadeh, A., Ostadrahimi, H., Ohadi, M. A. D., Saneei, S. A., & Ershadi, A. S. B. (2021) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2021.07.042 · Cited by 10
Quang, H., Wearne, T. A., Filipčíková, M., Pham, N., Nguyen, N., & McDonald, S. (2023) · Neuropsychology Review · doi:10.1007/s11065-023-09620-4 · Cited by 8
Specific mechanisms underlying executive and emotional apathy: A phenotyping study
Lafond-Brina, G., Pham, B., & Bonnefond, A. (2024) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2024.02.022 · Cited by 9
Apathy in corticobasal degeneration: possible parietal involvement
Moretti, R. (2017) · Functional Neurology · doi:10.11138/fneur/2017.32.4.201 · Cited by 8
“, 2015), although data remain controversial (Huang et al., 2013; Skidmore et al., 2013; Kos et al., 2016; Moretti and Signori, 2016).”
BackgroundRaffard, S., Bortolon, C., Yazbek, H., Lançon, C., Benoît, M., Norton, J. L., & Capdevielle, D. (2018) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-018-0907-1 · Cited by 8
Apathy in depression: An arterial spin labeling perfusion MRI study
Batail, J.-M. V., Corouge, I., Combès, B., Conan, C., Guillery-Sollier, M., Vérin, M., Sauleau, P., Jeune, F. L., Gauvrit, J., Robert, G., et al. (2022) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2022.11.015 · Cited by 10
“…of daily living (Freels et al., 1992), cognitive impairment with executive dysfunction (Zahodne and Tremont, 2013), increased risk of conversion to dementia (Vicini Chilovi et al., 2009), decreased response to treatment (Kos et al., 2016) and diminished quality of life (Prakash et al., 2016).”
Apathy is not associated with a panel of biomarkers in older adults with HIV disease
Woods, S. P., Thompson, J. L., Babicz, M. A., Shahani, L., Colpo, G. D., Rocha, N. P., Morgan, E. E., & Teixeira, A. L. (2021) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2021.110666 · Cited by 7
Fu, X., Yang, X.-L., Cui, X.-L., Liu, F., Li, H.-B., Yan, M.-Q., Xie, G.-R., & Guo, W.-B. (2022) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2022.07.043 · Cited by 6
Jackson, M. G., & Robinson, E. S. J. (2022) · Emerging Topics in Life Sciences · doi:10.1042/etls20220004 · Cited by 12
Motomura, K., Kawamura, A., Ohka, F., Aoki, K., Nishikawa, T., Yamaguchi, J., Kibe, Y., Shimizu, H., Maeda, S., & Saito, R. (2023) · Journal of Neuropsychology · doi:10.1111/jnp.12345 · Cited by 6
Post-stroke apathy: A case series investigation of neuropsychological and lesion characteristics
Horne, K., Gibson, E. C., Byrne, J., Bender, J. R., & Robinson, G. A. (2022) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2022.108244 · Cited by 5
Caudate volume and symptoms of apathy in older adults with multiple sclerosis
Cote, S. E., Wagshul, M. E., Foley, F. W., Lipton, M. L., & Holtzer, R. (2023) · Multiple Sclerosis Journal · doi:10.1177/13524585231188096 · Cited by 5
Gao, Y., Meng, L., Lu, Z., Li, X., Luo, R.-Q., Lin, H., Pan, Z.-M., Xu, B., Huang, Q.-K., Xiao, Z., et al. (2025) · World Journal of Psychiatry · doi:10.5498/wjp.v15.i4.100289 · Cited by 5
Franz, M., Kebets, V., Berg, X., Georgiadis, F., Milano, B. A., Burrer, A., Brakowski, J., Kaiser, S., Seifritz, E., Homan, P., et al. (2025) · Schizophrenia Bulletin · doi:10.1093/schbul/sbaf078 · Cited by 6
“37,38 39 morphometric findings on striatal subregions have been inconsistent, with studies reporting negative , 40, 41 positive, 42 or Integrating multiple lines of research, our study investigates whether localized OFC thickness alterations and OFC covariance networks constitute transdiagnostic…”
[Apathy in depression: a morphometric analysis].
Avedisova, A., Samotaeva, I., Luzin, R., Semenovyh, N. S., Sergunova, K., Akzhigitov, R., & Zakharova, R. V. (2019) · Zhurnal Nevrologii i Psikhiatrii imeni S.S. Korsakova · doi:10.17116/jnevro2019119051141 · Cited by 4
Apathetic symptoms and white matter integrity after traumatic brain injury
Navarro-Main, B., Castaño-Leon, A., Hilario, A., Lagares, A., Rubio, G., Periañez, J., Ríos-Lago, M., & Inertia Group Collaborators (2021) · Brain Injury · doi:10.1080/02699052.2021.1953145 · Cited by 5
Liu, Y., Hsien, Y.-K., Su, W., Tang, Z., Li, H., Long, J., Liao, X., & Zhang, H. (2025) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2025.1458602 · Cited by 4
Apathy as a failure of active inference
Williams, R. S., & Rowe, J. B. (2025) · Trends in Neurosciences · doi:10.1016/j.tins.2025.10.010 · Cited by 3
Perri, R., Carlesimo, G., & Costa, A. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.08.013 · Cited by 3
Daumas, L., Zory, R., Junquera-Badilla, I., y Montesino, M. F., Ettore, É., Robert, P. H., Sacco, G., Manera, V., & Ramanoël, S. (2023) · npj Aging · doi:10.1038/s41514-023-00121-5 · Cited by 3
Grayson, E. W., Xeni, F., Marangoni, C., & Jackson, M. G. (2025) · Current Protocols · doi:10.1002/cpz1.70195 · Cited by 2
“Disorders of motivation such as apathy syndrome are highly prevalent across a wide range of neurological and neurodegenerative disorders and can profoundly impact quality of life and disease progression (Chase, 2011; Kos et al., 2016; Malpetti et al., 2021; Zhu et al., 2019).”
Kesserwani, H. N. (2021) · Cureus · doi:10.7759/cureus.13802 · Cited by 3
“The inferior parietal cortex has also been implicated [7].”
BackgroundPoletti, B., Solca, F., Maffi, S., Torre, S., Carelli, L., Aiello, E. N., Ferrucci, R., Priori, A., Monti, A., Verde, F., et al. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1031908 · Cited by 3
“, 2020) as a consequence of altered cortical and/or subcortical, frontal-parietal circuitries (Kos et al., 2016; Raimo et al., 2019).”
BackgroundKreshpa, W., Raffa, S., Girtler, N. G., Brugnolo, A., Mattioli, P., Orso, B., Calizzano, F., Arnaldi, D., Peira, E., Chincarini, A., et al. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-240430 · Cited by 5
Varchetta, M. (2024) · doi:10.3390/brainsci14101003 · Cited by 2
“This may be due to the burden of disease symptoms, but also the presence of extracerebellar signs indicates the involvement of extracerebellar brain structures, including the fronto-subcortical circuits, which are linked to the pathogenesis of apathy [39,46].”
BackgroundNorris, S., Salgado, F., Murray, S., Amen, D., & Keator, D. B. (2025) · Depression and Anxiety · doi:10.1155/da/2739947 · Cited by 4
Apathy in persons with neurocognitive disorders: Moving the field forward
Gatchel, J. R., Husain, M., Brodaty, H., Burhan, A. M., Manera, V., Nijsten, J. M. H., Zhu, C. W., Gastiazoro, M. P., & Lanctôt, K. L. (2026) · International Psychogeriatrics · doi:10.1016/j.inpsyc.2026.100240 · Cited by 2
An Exploratory Comparison of Alpha and Beta Network Connectivity Across Four Depression Subtypes
Sharpley, C. F., Evans, I. D., Bitsika, V., Vessey, K. A., Odierna, G. L., Jesulola, E., & Agnew, L. L. (2025) · Journal of Clinical Medicine · doi:10.3390/jcm14155295 · Cited by 2
“The depressed sample showed two connectivity pairs from the right lateral parietal lobule (DMN), which has often been linked with increased apathy in a range of disorders [16,76,77].”
Liang, Y., Chen, L., Cao, Q., Lin, W., Guo, Q., & Wang, Y. (2019) · Current Psychology · doi:10.1007/s12144-019-00243-8 · Cited by 1
de Bruin, J., Kopell, B., Mayberg, H., Jimenez-shahed, J., Beudel, M., Choi, K. S., & Figee, M. (2026) · Brain Stimulation · doi:10.1016/j.brs.2026.103183 · Cited by 1
Apathy in Parkinson’s Disease: EEG Microstate Characteristics
Tungaç, F. Ç., Toplutaş, E., Mantar, N., Güntekin, B., & Hanoğlu, L. (2025) · Brain Topography · doi:10.1007/s10548-025-01124-z · Cited by 1
“…microstates was (2016) also describe the anatomical substrates of Parkinsonian apathy as distributed in the frontal and parietal regions, including the superior, middle, inferior, orbitofrontal gyri, anterior cingulate cortex (ACC), inferior parietal cortex, precuneus, and cuneus (Kos et al. 2016).”
rTMS for treatment of negative symptoms in schizophrenia: Clinical effects and neural basis
Lavallé, L., & Aleman, A. (2019) · L Encéphale · doi:10.1016/j.encep.2019.04.002 · Cited by 1
Self-citationFranz, M., Kebets, V., Berg, X., Georgiadis, F., Burrer, A., Brakowski, J., Kaiser, S., Seifritz, E., Homan, P., Walton, E., et al. (2024) · medRxiv · doi:10.1101/2024.07.29.24311172 · Cited by 1
Apathy as a Loss of Prior Precision on Action OutcomesPreprint
Williams, R. S., Naessens, M., Jafarian, A., Lanskey, J. H., Hezemans, F. H., Friston, K. J., Hughes, L. E., & Rowe, J. B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.06.680685 · Cited by 1
“Both regions have also been associated with apathy and impulsivity 31 – 33 with the orbitofrontal cortex playing a central role in updating stimulus value through contextualising sensory input 34 , and the medial prefrontal cortex representing behavioural contexts 35 crucial to action selection and…”
Portegies, M. L. P. (2020) · Bohn Stafleu van Loghum eBooks · doi:10.1007/978-90-368-2549-8_9
Martinez, E. S. (2022) · Gredos (University of Salamanca) · doi:10.14201/gredos.150999
Preserved reward sensitivity following acquired brain injury: A pilot study in acute rehabilitationPreprint
Magee, K., Cohen‐Zimerman, S., Grafman, J. H., & Roth, E. J. (2024) · doi:10.31234/osf.io/nt2y3
Emotional and volitional disorders after stroke
Пизова, Н. В., & Pizov, A. V. (2025) · Russian neurological Journal · doi:10.30629/2658-7947-2025-30-4-4-9
van Dorst, M. E. G., Roosenschoon, J., Nijsten, J. M. H., Plouvier, A. O. A., Koopmans, R. T. C. M., Gerritsen, D. L., Rensen, Y. C. M., & Kessels, R. P. C. (2025) · Geriatrics · doi:10.3390/geriatrics10060146
“A cross-population literature review shows that—in addition to population-specific brain abnormalities underlying apathy—abnormalities within the frontostriatal circuitry, the anterior cingulate cortex, and the inferior parietal cortex are associated with apathy in different populations [10].”
Rethinking apathy assessment in neurological disorders: conceptual and clinical challenges
Noreña, D. D., Lago, M. R., Adrover‐Roig, D., & Cubillo, I. S. (2026) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/acag030
Apathy and resting state functional connectivity across the Alzheimer's disease continuum
Rivera‐Delpin, G., Palmer, P., Ramseyer, M., Aibel, C. R., Yu, M., Munro, C. E., Vannini, P., Gatchel, J. R., & Marshall, G. A. (2026) · Alzheimer s & Dementia Diagnosis Assessment & Disease Monitoring · doi:10.1002/dad2.70378
“…structural and metabolic alterations in regions such as the dorsal anterior cingulate cortex, prefrontal cortex, basal ganglia, temporal lobes, and lateral parietal cortex have been associated with apathy, 18,29–32 the corresponding changes in functional connectivity are not yet well understood.”
Metadata
- Authors
- Kos, C., van Tol, M.-J., Marsman, J.-B. C., Knegtering, H., & Aleman, A.
- Affiliations
- University Medical Center Groningen (NL)
- Corresponding author
- Kos, Claire
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2016-10
- Volume
- 69
- Pages
- 381-401
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2514186414
- Cited by
- 101
- References
- 130
- Citations by year
- 2026: 6 · 2025: 12 · 2024: 6 · 2023: 10 · 2022: 8 · 2021: 11 · 2020: 15 · 2019: 5 · 2018: 15 · 2017: 12 · 2016: 1
- FWCI
- 1.17
- Type
- journal article
- Language
- en
- Open access
- green
- research.rug.nl
- Licence
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (312787, 453-11-004, 016156077)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- apathy, neural correlates, neurodegenerative diseases, acquired brain injury, mental illness, frontostriatal circuits, inferior parietal cortex, goal-directed behavior, intention, goal selection, action planning
- MeSH terms
- Mental Disorders, Brain, Brain Injuries, Humans, Neurodegenerative Diseases, Apathy
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