Neurobiological correlates of apathy in alzheimer's disease and mild cognitive impairment: A critical review

Journal of Alzheimer's Disease

Volumn 39, Issue 3, 2014, Pages 633-648

  Stella, Florindo ^a,b   Radanovic, Márcia ^b   Aprahamian, Ivan ^b   Canineu, Paulo Renato ^b,c   De Andrade, Larissa Pires ^a   Forlenza, Orestes Vicente ^b  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c PONTIFÍCIA UNIVERSIDADE CATÓLICA DE SÃO PAULO   (Brazil)

Author keywords

Alzheimer's disease; Apathy; mild cognitive impairment; neurobiological correlates; neuroimaging; review

Indexed keywords

BIOLOGICAL MARKER;

ALZHEIMER DISEASE; ANTERIOR CINGULATE; APATHY; ARTICLE; BRAIN REGION; CLINICAL ASSESSMENT; COGNITION; CORRELATION ANALYSIS; EVIDENCE BASED PRACTICE; HUMAN; MILD COGNITIVE IMPAIRMENT; NEUROBIOLOGY; NEUROIMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; SYSTEMATIC REVIEW;

ALZHEIMER'S DISEASE; APATHY; MILD COGNITIVE IMPAIRMENT; NEUROBIOLOGICAL CORRELATES; NEUROIMAGING; REVIEW;

ALZHEIMER DISEASE; APATHY; BRAIN; HUMANS; MILD COGNITIVE IMPAIRMENT; NEUROBIOLOGY; PUBMED; STATISTICS AS TOPIC;

EID: 84894113323     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-131385     Document Type: Article

References (59)

1. Aalten P, Verhey FRJ, Boziki M, Bullock R, Byerne EJ, Camus V, Caputo M, Collins D, Deyn PP, Elina K, Frisoni G, Girtler N, Holmes C, Hurt C, Marriott A, Mecocci P, Nobili F, Ousset PJ, Reynish E, Salmon E, Tsolak M, Vellas B, Robert PH (2007) Neuropsychiatric Syndromes in dementia. Dement Geriatr Cogn Disord 24, 457-463.
2. De Medeiros K Robert P, Gauthier S, Stella F, Politis A Leoutsakos J, Taragano F, Kremer J, Brugnolo A, Porsteins-son AP, Geda YE, Brodaty H, Gazdag G, Cummings J, Lyketsos C, and the NPI-C Research Group (2010) The Neuropsychiatric Inventory-Clinician rating scale (NPI-C): Reliability and validity of a revised assessment of neu-ropsychiatric symptoms in dementia. Int Psychogeriatr 22, 984-994.
3. Mulin E, Leone E, Dujardin K, Delliaux M, Leentjens A, Nobili F, Dessi B, Tible O, Aguera-Ortiz L, Osorio RS, Yessavage J, Dachevsky D, Verhey FRJ, Jentoft AJC, Blanc O, Llorca PM, Robert PH (2011) Diagnostic criteria for apathy in clinical practice. Int J Geriatr Psychiatry 26, 158-165.
4. Di Iulio F, Palmer K, Blundo C, Casini AR, Gianni W, Caltagirone C, Spalletta G (2010) Occurrenceofneuropsychi-atric symptoms and psychiatric disorders in mild Alzheimer's disease and mild cognitive impairment subtypes. Int Psy-chogeriatr 22, 629-640.
5. Stella F, Andrade LP, Garuffi M, Vital TM, Hernández SSS, Ruocco M, Sé EVG, Klein M, Martins T, Robert PH (2013) Validation of the Brazilian version of the Apathy Inventory. Int J Geriatr Psychiatry 28, 979-986.
6. Robert PH, Darcourt G, Koulibaly MP, Clairet S, Benoit M, Garcia R, Dechaux O, Darcourt J (2006) Lack of initiative and interest in Alzheimer's disease: A single photon emission computed tomography study. Eur J Neurol 13, 729-735.
7. Stella F, Forlenza OV, Laks J, Andrade LP, Avendaño MAL, Sé EVG, Cação JC, Lyketsos CG, de Medeiros K (2013) The Brazilian version ofthe Neuropsychiatric Inventory-Clinician rating (NPI-C): Reliability and validity in dementia. Int Psy-chogeriatr 25, 1503-1511.
8. Lechowski L, Benoit M, Chassagne P, Vedel I, Tortrat D, Teillet L, Vellas B (2009) Persistent apathy in Alzheimer's disease as an independent factor of rapid functional decline: The REAL longitudinal cohort study. Int J Geriatr Psychiatry 24, 341-346.
9. Starkstein SE, Mizrahi R, Capizzano AA, Acion L, Brock-man S, Power BD (2009) Neuroimaging correlates of apathy and depression in Alzheimer's disease. J Neuropsychiatr Clin Neurosci 21, 259-265.
10. Robert PH, Mulin E, Malle P, David R (2010) Apathy diagnosis, assessment, and treatment in Alzheimer's disease. CNS Neurosci Ther 16, 263-271.
11. Lyketsos CG (2007) Neuropsychiatric symptoms (behavioral and psychological symptoms of dementia) and development of dementia treatments. Int Psychogeriatrics 19, 409-420.
12. Cummings JL, Mackell J, Kaufer D (2008) Behavioral effectsofcurrent Alzheimer's diseasetreatment:Adescriptive review. Alzheimer Dement 4, 49-60.
13. Gauthier S, Cummings J, Ballard C, Brodaty H, Grosberg G, Robert P, Lyketsos C (2010) Management of behavioral problems in Alzheimer's disease. Int Psychogeriatr 22, 346-372.
14. Robert P, Berr C, Volteau M, Bertogliati C, Benoit M, Mahieux F, Legrain S, Dubois B, Study PréAL (2006) Neu-ropsychological performance in mild cognitive impairment with and without apathy. Dement Geriatr Cogn Disord 21, 192-197.
15. Kim JW, Lee DY, Choo IH, Seo EH, Kim SG, Park SY, Woo JI (2011) Microstructural alteration of the anterior cingulum is associated with apathy in Alzheimer disease. Am J Geriatr Psychiatry 19, 644-653.
16. Kang JY, Lee JS, Kang H, Lee HW, Kim YK, Jeon HJ, Chung JK, Lee MC, Cho MJ, Lee DS (2012) Regional cerebral blood flow abnormalities associated with apathy and depression in Alzheimer's disease. Alzheimer Dis Assoc Disord 26, 217-224.
17. Benoit M, Koulibaly PM, Migneco O, Darcourt J, Pringuey DJ, Robert PH (2002) Brain perfusion in Alzheimer's disease with and without apathy: A SPECT study with statistical parametric mapping analysis. Psychiatry Res 114, 103-111.
18. Tunnard C, Whitehead D, Hurt C, Wahlund LO, Mecocci P, Tsolaki M, Vellas B, Spenger C, Kłoszewska I, Soininen H, Lovestone S, Simmons A, on behalf of the AddNeu-roMed Consortium (2011) Apathy and cortical atrophy in Alzheimer's disease. Int J Geriatr Psychiatry 26, 741-748.
19. Jonsson M, Edman A, Lind K, Rolstad S, Sjogren M, Wallin A (2010) Apathy is a prominent neuropsychiatric feature of radiological white-matter changes in patients with dementia. Int J Geriatr Psychiatry 25, 588-595.
20. Cacciari C, Moraschia M, Di Paola M, Cherubini A, Orfeia MD, Giove F, Maraviglia B, Caltagirone C, Spalle G (2010) White Matter Microstructure and Apathy Level in Amnestic Mild Cognitive Impairment. J Alzheimers Dis 2, 501-507.
21. Vercelletto M, Martinez F, Lanier S, Magne C, Jaulin P, Bourin M (2002) Negative symptoms, depression and Alzheimer's disease. Int J Geriatr Psychiatry 17, 383-387.
22. Craig AH, Cummings JL, Fairbanks L, Itti L, Miller BL, Li L, Mena I (1996) Cerebral blood flow correlates of apathy in Alzheimer disease. Arch Neurol 53, 1116-1120.
23. Ott BR, Noto RB, Fogel BS (1996) Apathy and loss of insight in Alzheimer's disease: A SPECT imaging study. J Neuropsy-chiatr Clin Neurosci 8, 41-46.
24. Starkstein SE, Sabe L, Vásquez S, Di Lorenzo G, Mart́inez A, Petracca G, Tesón A, Chemerinski E, Leiguarda R (1997) Neuropsychological, psychiatric, and cerebral perfusion correlates of leukoaraiosis in Alzheimer's disease. J Neurol Neurosurg Psychiatry 63, 66-73.
25. Benoit M, Dygai I, Migneco O, Robert PH, Bertogliati C, Darcourt J, Benoliel J, Aubin-Brunet V, Pringuey D (1999) Behavioral and psychological symptoms in Alzheimer's disease: Relation between apathy and regional cerebral per-fusion. Dement Geriatr Cogn Disord 10, 511-517.
26. Migneco O, Benoit M, Koulibaly PM, Dygai I, Bertogliati C, Desvignes P, Robert PH, Malandain G, Bussiere F, Darcourt J (2001) Perfusion brain SPECT and statistical parametric mapping analysis indicate that apathy is a cingulate syndrome: A study in Alzheimer's disease and nondemented patients. Neuro Image 13, 896-902.
27. Benoit M, Clairet S, Koulibaly PM, Darcourt J, Robert PH (2004) Brain perfusion correlates of the Apathy Inventory dimensions of Alzheimer's disease. Int J Geriatr Psychiatry 19, 864-869.
28. Thomas P, Hazif-Thomas C, Saccardy F, Vandermarq P (2004) Démotivation et dysfonctionnements frontaux chez le sujet âgé: Place de la leucoaräiose. Encephale 30, 52-59.
29. Holthoff VA, Beuthien-Baumann B, Kalbe E, Lüdecke S, Lenz O, Zündorf G, Sperling R, Schierz K, Winiecki P, Sorbi S, Herholz K (2005) Regional cerebral metabolism in early Alzheimer's disease with clinically significant apathy or depression. Biol Psychiatry 57, 412-421.
30. Lanctôt KL, Moosa S, Herrmann N, Leibovitch FS, Rothen-burg L, Cotter A, Black SE (2007) A SPECTstudy of apathy in Alzheimer's disease. Dement Geriatr Cogn Disord 24, 65-72.
31. Marshall GA, Monserratt L, Harwood D, Mandelkern M, Cummings JL, Sultzer DL (2007) Positron emission tomography metabolic correlates of apathy in Alzheimer disease. Arch Neurol 64, 1015-1020.
32. Apostolova LG, Akopyan GG, Partiali N, Steiner CA, Dut-ton RA, Hayashi KM, Dinov ID, Toga AW, Cummings JL, Thompson PM (2007) Structural correlates of apathy in Alzheimer's disease. Dement Geriatr Cogn Disord 24, 91-97.
33. Padala PR, Stevens A, Boska M, Sengel S, Petty F, Burke W (2007) Magnetic resonance spectroscopy study of apathy in Alzheimer's dementia. J Am Geriatr Soc 55 (Suppl. S1), S153-S153.
34. Bruen PD, McGeown WJ, Shanks MF, Venneri A (2008) Neuroanatomical correlates of neuropsychiatric symptoms in Alzheimer's disease. Brain 131, 2455-2463.
35. David R, Koulibaly M, Benoit M, Garcia R, Caci H, Darcourt J, Robert P (2008) Striatal dopamine transporter levels correlate with apathy in neurodegenerative diseases A SPECT study with partial volume effect correction. Clin Neurol Neu-rosurg 110, 19-24.
36. Ota M, Sato N, Nakata Y, Arima K, Uno M (2012) Relationship between apathy and diffusion tensor imaging metrics of the brain in Alzheimer's disease. Int J Geriatr Psychiatry 27, 722-726.
37. Balthazar MLF, Pereira FRS, Lopes TM, Silva EL, Coan AC, Campos BM, Stella F, Damasceno BP, Cendes F (2013) Neuropsychiatric syndromes in AD are related to functional connectivity alterations in default mode and salience networks. Hum Brain Mapp, doi: 10.1002/hbm.22248.
38. Zahodne LB, Gongvatana A, Cohen A, Ott BR, Tremont G, Alzheimer's Disease Neuroimaging, Initiative (2013) Are apathy and depression independently associated with longitudinal trajectories of cortical atrophy in mild cognitive impairment? Am J Geriatr Psychiatry 21, 1098-1106.
39. Forstl H, Burns A, Levy R, Cairns N, Luthert P, Lantos P (1993) Neuropathological correlates of behavioral disturbance in confirmed Alzheimer's disease. Br J Psychiatry 163, 364-368.
40. Tekin S, Mega MS, Masterman DM, Chow T, Garakian J, Vinters HV, Cummings JL (2001) Orbitofrontal and anterior cingulate cortex neurofibrillary tangle burden is associated with agitation in Alzheimer disease. Ann Neurol 49, 355-361.
41. Monastero R, Mariani E, Camarda C, Ingegni T, Averna MR, Senin U, Camarda R, Mecocci P (2006) Association between apolipoprotein E e4 allele and apathy in probable Alzheimer's disease. Acta Psychiatr Scand 113, 59-63.
42. Marshall GA, Fairbanks LA, Tekin S, Harry V, Vinters HV, Cummings JC (2006) Neuropathologic correlates of apathy in Alzheimer's disease. Dement Geriatr Cogn Disord 21, 144-147.
43. Skogseth R, Mulugeta E, Jones E, Ballard C, Rongve A, Nore S, Alves G, Aarsland D (2008) Neuropsychiatric corre-latesofcerebrospinalfluid biomarkersinAlzheimer's disease. Dement Geriatr Cogn Disord 25, 559-563.
44. Reeves S, Brown R, Howard Grasby P (2009) Increased stri-atal dopamine (D2/D3) receptor availability and delusions in Alzheimer disease. Neurology 72, 528-534.
45. Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J (1994) The Neuropsychiatric Inventory: Comprehensive assessment of psychopathology in dementia. Neurology 44, 2308-2314.
46. Robert PH, Clairet S, Benoit M, Koutaich J, Bertogliati C Tible O, Caci H, Borg M, Brocker P, Bedoucha P (2002) The Apathy Inventory: Assessment of apathy and awareness in Alzheimer's disease, Parkinson's disease and mild cognitive impairment. Int J Geriatr Psychiatry 17, 1099-1105.
47. Marin RS, Biedrzycki RC, Firinciogullari S (1991) Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res 38, 143-162.
48. Starkstein SE, Mayberg HS, Preziosi TJ, Andrezejewski P, Leiguarda R, Robinson RG (1992) Reliability, validity, and clinical correlates of apathy in Parkinson's disease. J Neu-ropsychiatr Clin Neurosci 4, 134-139.
49. Dubois B, Slachevsky A, Litvan I, Pillon B (2000) The FAB: A Frontal Assessment Battery at bedside. Neurology 55, 1621-1626.
50. Cardebat D, Doyon B, Puel M, Goulet P, Joanette Y (1990) Evocation lexicale formelle etsémantique chez des sujets nor-maux: Performances et dynamique de production en fonction du sexe, de l'age et du niveau d'étude. Acta Neurol Belg 90, 207-217.
51. McPherson S, Fairbanks L, Tiken S, Cummings JL, Back-Madruga C (2002) Apathy and executive function in Alzheimer's disease. J Int Neuropsychol Soc 8, 373-381.
52. Levy R, Dubois B (2006) Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cerebr Cortex 16, 916-928.
53. Wallis JD (2007) Orbitofrontal cortex and its contribution to decision-making. Annu Rev Neurosci 30, 31-56.
54. Verghese PB, Castellano JM, Holtzman DM (2011) Apolipoprotein E in Alzheimer's disease and other neurological disorders. Lancet Neurol 10, 241-252.
55. Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118, 279-306.
56. Levy ML, Cummings JL, Fairbanks LA, Masterman D, Miller BL, Craig AH, Paulsen JS, Litvan I (1998) Apathy is not depression. J Neuropsychiatr Clin Neurosci 10, 314-319.
57. Voineskos NA, Rajji TK, Lobaugh NJ, Miranda D, Shenton ME, Kennedy JL, Pollock BG, Mulsant BH (2012) Age-related decline in white matter tract integrity and cognitive performance: A DTI tractography and structural equation modeling study. Neurobiol Aging 33, 21-34.
58. Torralva T, Roca M, Gleichgerrcht E, Bekinschtein T, Manes F (2009) A neuropsychological battery to detect specific executive and social cognitive impairments in early frontotemporal dementia. Brain 132, 1299-1309.
59. Funkiewiez A, Bertoux M, de Souza LC, Levy R, Dubois B (2012) The SEA (Social cognition and Emotional Assessment): A clinical neuropsychological tool for early diagnosis of frontal variant of frontotemporal lobar degeneration. Neu-ropsychology 26, 81-90.