دورية أكاديمية
Anatomical correlates of apathy and impulsivity co-occurrence in early Parkinson's disease.
| العنوان: | Anatomical correlates of apathy and impulsivity co-occurrence in early Parkinson's disease. |
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| المؤلفون: | Maggi G; Department of Psychology, University of Campania 'Luigi Vanvitelli', Caserta, Italy., Loayza F; Neurosciences and Bioengineering Laboratory, Faculty of Mechanical and Production Sciences Engineering, Polytechnic University (ESPOL), Guayaquil, Ecuador., Vitale C; Department of Medical, Motor Sciences and Wellness, University 'Parthenope', Naples, Italy.; Institute of Diagnosis and Health, IDC-Hermitage Capodimonte, Naples, Italy., Santangelo G; Department of Psychology, University of Campania 'Luigi Vanvitelli', Caserta, Italy., Obeso I; HM-CINAC, Centro Integral de Neurociencias AC. HM Hospitales, Av. Carlos V, 70, Móstoles, 28938, Madrid, Spain. i.obesomartin@gmail.com.; CINC, CSIC, Madrid, Spain. i.obesomartin@gmail.com. |
| المصدر: | Journal of neurology [J Neurol] 2024 May; Vol. 271 (5), pp. 2798-2809. Date of Electronic Publication: 2024 Feb 28. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 0423161 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-1459 (Electronic) Linking ISSN: 03405354 NLM ISO Abbreviation: J Neurol Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Berlin ; New York, Springer-Verlag |
| مواضيع طبية MeSH: | Parkinson Disease*/complications , Parkinson Disease*/pathology , Parkinson Disease*/diagnostic imaging , Parkinson Disease*/physiopathology , Apathy*/physiology , Magnetic Resonance Imaging* , Gray Matter*/diagnostic imaging , Gray Matter*/pathology , Disruptive, Impulse Control, and Conduct Disorders*/etiology , Disruptive, Impulse Control, and Conduct Disorders*/physiopathology , Disruptive, Impulse Control, and Conduct Disorders*/diagnostic imaging , Disruptive, Impulse Control, and Conduct Disorders*/pathology, Humans ; Male ; Female ; Middle Aged ; Aged ; Longitudinal Studies ; Impulsive Behavior/physiology |
| مستخلص: | Background: Although apathy and impulse control disorders (ICDs) are considered to represent opposite extremes of a continuum of motivated behavior (i.e., hypo- and hyperdopaminergic behaviors), they may also co-occur in Parkinson's disease (PD). Objectives: We aimed to explore the co-occurrence of ICDs and apathy and its neural correlates analyzing gray matter (GM) changes in early untreated PD patients. Moreover, we aimed to investigate the possible longitudinal relationship between ICDs and apathy and their putative impact on cognition during the first five years of PD. Methods: We used the Parkinson's Progression Markers Initiative (PPMI) database to identify the co-occurrence of apathy and ICDs in 423 early drug-naïve PD patients at baseline and at 5-year follow-up. Baseline MRI volumes and gray matter changes were analyzed between groups using voxel-based morphometry. Multi-level models assessed the longitudinal relationship (across five years) between apathy and ICDs and cognitive functioning. Results: At baseline, co-occurrence of apathy and ICDs was observed in 23 patients (5.4%). This finding was related to anatomical GM reduction along the cortical regions involved in the limbic circuit and cognitive control systems. Longitudinal analyses indicated that apathy and ICDs were related to each other as well as to the combined use of levodopa and dopamine agonists. Worse apathetic and ICDs states were associated with poorer executive functions. Conclusions: Apathy and ICDs are joint non-exclusive neuropsychiatric disorders also in the early stages of PD and their co-occurrence was associated with GM decrease in several cortical regions of the limbic circuit and cognitive control systems. (© 2024. The Author(s).) |
| References: | Weintraub D, Mamikonyan E (2019) The neuropsychiatry of Parkinson disease: a perfect storm. Am J Geriatr Psychiatry 27(9):998–1018. (PMID: 10.1016/j.jagp.2019.03.002310065507015280) American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Association. (PMID: 10.1176/appi.books.9780890425596) Marin RS (1991) Apathy: a neuropsychiatric syndrome. J Neuropsychiatry Clin Neurosci 3:243–254. (PMID: 10.1176/jnp.3.3.2431821241) Stenberg G (2016) Impulse control disorders: the continuum hypothesis. J Parkinsons Dis 6:67–75. https://doi.org/10.3233/JPD-150770. (PMID: 10.3233/JPD-15077027031861) Petitet P, Scholl J, Attaallah B et al (2021) The relationship between apathy and impulsivity in large population samples. Sci Rep. https://doi.org/10.1038/s41598-021-84364-w. (PMID: 10.1038/s41598-021-84364-w336493997921138) Ahearn DJ, McDonald K, Barraclough M, Leroi I (2012) An exploration of apathy and impulsivity in Parkinson disease. Curr Gerontol Geriatr Res. https://doi.org/10.1155/2012/390701. (PMID: 10.1155/2012/390701228298143399379) Leroi I, Harbishettar V, Andrews M et al (2012) Carer burden in apathy and impulse control disorders in Parkinson’s disease. Int J Geriatr Psychiatry. https://doi.org/10.1002/gps.2704. (PMID: 10.1002/gps.270421462269) Palmeri R, Corallo F, Bonanno L et al (2022) Apathy and impulsiveness in Parkinson disease: two faces of the same coin? Medicine 101:e29766. https://doi.org/10.1097/MD.0000000000029766. (PMID: 10.1097/MD.0000000000029766357769859239641) Scott BM, Eisinger RS, Burns MR et al (2020) Co-occurrence of apathy and impulse control disorders in Parkinson disease. Neurology. https://doi.org/10.1212/WNL.0000000000010965. (PMID: 10.1212/WNL.0000000000010965332685577734726) Gatto EM, Aldinio V (2019) Impulse control disorders in Parkinson’s disease. A brief and comprehensive review. Front Neurol. https://doi.org/10.3389/fneur.2019.00351. (PMID: 10.3389/fneur.2019.00351310574736481351) Pagonabarraga J, Kulisevsky J, Strafella AP, Krack P (2015) Apathy in Parkinson’s disease: clinical features, neural substrates, diagnosis, and treatment. Lancet Neurol 14:518–531. (PMID: 10.1016/S1474-4422(15)00019-825895932) Santangelo G, Raimo S, Cropano M et al (2019) Neural bases of impulse control disorders in Parkinson’s disease: a systematic review and an ALE meta-analysis. Neurosci Biobehav Rev 107:672–685. (PMID: 10.1016/j.neubiorev.2019.09.04131586557) Husain M, Roiser JP (2018) Neuroscience of apathy and anhedonia: a transdiagnostic approach. Nat Rev Neurosci 19(8):470–484. (PMID: 10.1038/s41583-018-0029-929946157) Girard R, Obeso I, Thobois S et al (2019) Wait and you shall see: sexual delay discounting in hypersexual Parkinson’s disease. Brain. https://doi.org/10.1093/brain/awy298. (PMID: 10.1093/brain/awy29831603507) Cerasa A, Salsone M, Nigro S et al (2014) Cortical volume and folding abnormalities in Parkinson’s disease patients with pathological gambling. Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.2014.09.001. (PMID: 10.1016/j.parkreldis.2014.09.00125443555) Tessitore A, Santangelo G, De Micco R et al (2016) Cortical thickness changes in patients with Parkinson’s disease and impulse control disorders. Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.2015.10.013. (PMID: 10.1016/j.parkreldis.2015.10.01326810913) Tessitore A, Santangelo G, De Micco R et al (2017) Resting-state brain networks in patients with Parkinson’s disease and impulse control disorders. Cortex. https://doi.org/10.1016/j.cortex.2017.06.008. (PMID: 10.1016/j.cortex.2017.06.00828715675) Tessitore A, De Micco R, Giordano A et al (2017) Intrinsic brain connectivity predicts impulse control disorders in patients with Parkinson’s disease. Mov Disord. https://doi.org/10.1002/mds.27139. (PMID: 10.1002/mds.2713928949049) Reijnders JSAM, Scholtissen B, Weber WEJ et al (2010) Neuroanatomical correlates of apathy in Parkinson’s disease: a magnetic resonance imaging study using voxel-based morphometry. Mov Disord. https://doi.org/10.1002/mds.23268. (PMID: 10.1002/mds.2326820669264) Prange S, Metereau E, Maillet A et al (2019) Early limbic microstructural alterations in apathy and depression in de novo Parkinson’s disease. Mov Disord. https://doi.org/10.1002/mds.27793. (PMID: 10.1002/mds.2779331309609) Zhang Y, Wu J, Wu W et al (2018) Reduction of white matter integrity correlates with apathy in Parkinson’s disease. Int J Neurosci. https://doi.org/10.1080/00207454.2017.1347170. (PMID: 10.1080/00207454.2017.134717030375250) Baggio HC, Segura B, Garrido-Millan JL et al (2015) Resting-state frontostriatal functional connectivity in Parkinson’s disease-related apathy. Mov Disord 30:671–679. https://doi.org/10.1002/mds.26137. (PMID: 10.1002/mds.2613725600482) Chahine LM, Xie SX, Simuni T et al (2016) Longitudinal changes in cognition in early Parkinson’s disease patients with REM sleep behavior disorder. Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.2016.03.006. (PMID: 10.1016/j.parkreldis.2016.03.006270100705031362) Weintraub D, Papay K, Siderowf A (2013) Screening for impulse control symptoms in patients with de novo Parkinson disease: a casecontrol study. Neurology. https://doi.org/10.1212/WNL.0b013e31827b915c. (PMID: 10.1212/WNL.0b013e31827b915c241376263908465) Maggi G, Vitale C, Giacobbe C et al (2024) Validation of the Italian version of the questionnaire for impulsive-compulsive disorders in Parkinson’s disease - rating scale (QUIP-RS) in an Italian Parkinson’s disease cohort. Neurol Sci. https://doi.org/10.1007/s10072-024-07304-2. (PMID: 10.1007/s10072-024-07304-238418663) Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. https://doi.org/10.1002/hbm.1058. (PMID: 10.1002/hbm.105811747097) Kimmel DL, Elsayed GF, Cunningham JP, Newsome WT (2020) Value and choice as separable and stable representations in orbitofrontal cortex. Nat Commun. https://doi.org/10.1038/s41467-020-17058-y. (PMID: 10.1038/s41467-020-17058-y326513737351792) Howard JD, Kahnt T (2017) Identity-specific reward representations in orbitofrontal cortex are modulated by selective devaluation. J Neurosci 37:2627–2638. https://doi.org/10.1523/JNEUROSCI.3473-16.2017. (PMID: 10.1523/JNEUROSCI.3473-16.2017281599065354319) Mata-Marín D, Pineda-Pardo JÁ, Michiels M et al (2022) A circuit-based approach to modulate hypersexuality in Parkinson’s disease. Psychiatry Clin Neurosci. https://doi.org/10.1111/pcn.13523. (PMID: 10.1111/pcn.13523) Mosley PE, Paliwal S, Robinson K et al (2019) The structural connectivity of discrete networks underlies impulsivity and gambling in Parkinson’s disease. Brain. https://doi.org/10.1093/brain/awz327. (PMID: 10.1093/brain/awz327316652416439324) Narayana S, Laird AR, Tandon N et al (2012) Electrophysiological and functional connectivity of the human supplementary motor area. Neuroimage. https://doi.org/10.1016/j.neuroimage.2012.04.060. (PMID: 10.1016/j.neuroimage.2012.04.060225695433777814) Levy R, Dubois B (2006) Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Cortex 16(7):916–928. (PMID: 10.1093/cercor/bhj04316207933) Pellicano C, Niccolini F, Wu K et al (2015) Morphometric changes in the reward system of Parkinson’s disease patients with impulse control disorders. J Neurol. https://doi.org/10.1007/s00415-015-7892-3. (PMID: 10.1007/s00415-015-7892-326410743) Aarts E, Nusselein AAM, Smittenaar P et al (2014) Greater striatal responses to medication in Parkinson׳s disease are associated with better task-switching but worse reward performance. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2014.05.023. (PMID: 10.1016/j.neuropsychologia.2014.05.02324912070) Vitale C, Santangelo G, Trojano L et al (2011) Comparative neuropsychological profile of pathological gambling, hypersexuality, and compulsive eating in Parkinson’s disease. Mov Disord. https://doi.org/10.1002/mds.23567. (PMID: 10.1002/mds.2356722170277) Voon V, Napier TC, Frank MJ et al (2017) Impulse control disorders and levodopa-induced dyskinesias in Parkinson’s disease: an update. Lancet Neurol 16(3):238–250. (PMID: 10.1016/S1474-4422(17)30004-228229895) Santangelo G, Vitale C, Picillo M et al (2015) Apathy and striatal dopamine transporter levels in de-novo, untreated Parkinson’s disease patients. Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.2015.02.015. (PMID: 10.1016/j.parkreldis.2015.02.01526810913) Chung SJ, Lee JJ, Ham JH et al (2016) Apathy and striatal dopamine defects in non-demented patients with Parkinson’s disease. Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.2015.12.003. (PMID: 10.1016/j.parkreldis.2015.12.003276372845125780) Prange S, Metereau E, Maillet A et al (2022) Limbic serotonergic plasticity contributes to the compensation of apathy in early Parkinson’s disease. Mov Disord. https://doi.org/10.1002/mds.28971. (PMID: 10.1002/mds.2897135238430) Hezemans FH, Wolpe N, O’Callaghan C et al (2022) Noradrenergic deficits contribute to apathy in Parkinson’s disease through the precision of expected outcomes. PLoS Comput Biol 18:e1010079. https://doi.org/10.1371/journal.pcbi.1010079. (PMID: 10.1371/journal.pcbi.1010079355332009119485) Martini A, Dal Lago D, Edelstyn NMJ et al (2018) Dopaminergic neurotransmission in patients with Parkinson’s disease and impulse control disorders: a systematic review and meta-analysis of PET and SPECT studies. Front Neurol. https://doi.org/10.3389/fneur.2018.01018. (PMID: 10.3389/fneur.2018.01018306872086290338) Gearhardt AN, Yokum S, Orr PT et al (2011) Neural correlates of food addiction. Arch Gen Psychiatry. https://doi.org/10.1001/archgenpsychiatry.2011.32. (PMID: 10.1001/archgenpsychiatry.2011.32214643443980851) D’Iorio A, Maggi G, Vitale C et al (2018) “Pure apathy” and cognitive dysfunctions in Parkinson’s disease: a meta-analytic study. Neurosci Biobehav Rev 94:1–10. https://doi.org/10.1016/j.neubiorev.2018.08.004. (PMID: 10.1016/j.neubiorev.2018.08.00430114389) Santangelo G, D’Iorio A, Maggi G et al (2018) Cognitive correlates of “pure apathy” in Parkinson’s disease. Parkinsonism Relat Disord 53:101–104. https://doi.org/10.1016/j.parkreldis.2018.04.023. (PMID: 10.1016/j.parkreldis.2018.04.02329706433) Santangelo G, Raimo S, Barone P (2017) The relationship between impulse control disorders and cognitive dysfunctions in Parkinson’s disease: a meta-analysis. Neurosci Biobehav Rev 77:129–147. (PMID: 10.1016/j.neubiorev.2017.02.01828242338) Hinkle JT, Perepezko K, Mills KA, Pontone GM (2021) Attentional dysfunction and the punding spectrum in Parkinson’s disease. Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.2021.01.019. (PMID: 10.1016/j.parkreldis.2021.01.019348871739664995) Hinson JM, Jameson TL, Whitney P (2003) Impulsive decision making and working memory. J Exp Psychol Learn Mem Cogn. https://doi.org/10.1037/0278-7393.29.2.298. (PMID: 10.1037/0278-7393.29.2.29812696817) Mele B, Merrikh D, Ismail Z, Goodarzi Z (2019) Detecting Apathy in individuals with Parkinson’s disease: a systematic review. J Parkinsons Dis 9(4):653–664. (PMID: 10.3233/JPD-19161931424418) |
| فهرسة مساهمة: | Keywords: Addiction; Apathy; Impulse control disorders; Impulsivity; Neuropsychiatry; Parkinson’s disease |
| تواريخ الأحداث: | Date Created: 20240228 Date Completed: 20240427 Latest Revision: 20240705 |
| رمز التحديث: | 20240706 |
| مُعرف محوري في PubMed: | PMC11055726 |
| DOI: | 10.1007/s00415-024-12233-3 |
| PMID: | 38416170 |
| قاعدة البيانات: | MEDLINE |
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Full Text Finder | تدمد: | 1432-1459 |
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| DOI: | 10.1007/s00415-024-12233-3 |