Neuroimaging analysis of the dopamine basis for apathetic behaviors in an MPTP-lesioned primate model

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Tian, LinLin ^a   Xia, Yuanxuan ^a   Flores, Hubert P ^a   Campbell, Meghan C ^a,b   Moerlein, Stephen M ^b   Perlmutter, Joel S ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 2BETA CARBOMETHOXY 3BETA (4 FLUOROPHENYL)TROPANE C 11; 6 FLUORODOPAMINE F 18; DIHYDROTETRABENAZINE C 11; DOPAMINE; DOPAMINE TRANSPORTER; RADIOLIGAND; UNCLASSIFIED DRUG; RADIOPHARMACEUTICAL AGENT; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CINGULATE; APATHETIC BEHAVIOR; APATHY; ARTICLE; BEHAVIOR DISORDER; CELL COUNT; CONTROLLED STUDY; DISEASE SEVERITY; DOPAMINERGIC SYSTEM; DORSOLATERAL PREFRONTAL CORTEX; IN VITRO STUDY; IN VIVO STUDY; INSULA; MACACA FASCICULARIS; MACACA NEMESTRINA; MALE; MOTOR DYSFUNCTION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PARKINSONISM; POSITRON EMISSION TOMOGRAPHY; POSTERIOR CINGULATE; SUBSTANTIA NIGRA; TASK PERFORMANCE; VENTRAL TEGMENTUM; VENTROMEDIAL PREFRONTAL CORTEX; ANIMAL; ANTIBODY SPECIFICITY; BRAIN CORTEX; COMPARATIVE STUDY; DIAGNOSTIC IMAGING; DOPAMINERGIC NERVE CELL; METABOLISM; MOTIVATION; MOTOR ACTIVITY; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; SINGLE BLIND PROCEDURE;

ANIMALIA; PRIMATES;

ANIMALS; APATHY; CEREBRAL CORTEX; DOPAMINE; DOPAMINERGIC NEURONS; GOALS; MACACA FASCICULARIS; MACACA NEMESTRINA; MAGNETIC RESONANCE IMAGING; MALE; MOTOR ACTIVITY; NEUROIMAGING; ORGAN SPECIFICITY; PARKINSONIAN DISORDERS; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; SINGLE-BLIND METHOD; TYROSINE 3-MONOOXYGENASE;

EID: 84940062298     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132064     Document Type: Article

References (50)

1. Levy R, Czernecki V (2006) Apathy and the basal ganglia. J Neurol 253 Suppl 7: VII54-VII61. doi: 10.1007/s00415-006-7012-5 PMID: 17131230
2. Botzel K, Schulze S (1996) Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. Brain 119 (Pt 3): 1045-1048. PMID: 8673482
3. Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RS, Brooks DJ (1992) Impaired mesial frontal and putamen activation in Parkinson's disease: a positron emission tomography study. Ann Neurol 32: 151-161. PMID: 1510355
4. Reijnders JS, Scholtissen B, Weber WE, Aalten P, Verhey FR, Leentjens AF (2010) Neuroanatomical correlates of apathy in Parkinson's disease: A magnetic resonance imaging study using voxel-based morphometry. Mov Disord 25: 2318-2325. doi: 10.1002/mds.23268 PMID: 20669264
5. Samuel M, Ceballos-Baumann AO, Turjanski N, Boecker H, Gorospe A, Linazasoro G, et al. (1997) Pallidotomy in Parkinson's disease increases supplementary motor area and prefrontal activation during performance of volitional movements an H2(15)O PET study. Brain 120 (Pt 8): 1301-1313. PMID: 9278624
6. Skidmore FM, Yang M, Baxter L, von Deneen K, Collingwood J, He G, et al. (2013) Apathy, depression, and motor symptoms have distinct and separable resting activity patterns in idiopathic Parkinson disease. Neuroimage 81: 484-495. doi: 10.1016/j.neuroimage.2011.07.012 PMID: 21782030
7. Brown CA, Campbell MC, Karimi M, Tabbal SD, Loftin SK, Tian LL, et al. (2012) Dopamine pathway loss in nucleus accumbens and ventral tegmental area predicts apathetic behavior in MPTP-lesioned monkeys. Exp Neurol 236: 190-197. S0014-4886(12)00197-5 [pii]; doi: 10.1016/j.expneurol.2012.04.025 PMID: 22579525
8. Tabbal SD, Mink JW, Antenor JA, Carl JL, Moerlein SM, Perlmutter JS (2006) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced acute transient dystonia in monkeys associated with low striatal dopamine. Neuroscience 141: 1281-1287. S0306-4522(06)00620-8 [pii]; doi: 10.1016/j.neuroscience.2006.04.072 PMID: 16766129
9. Tian L, Karimi M, Loftin SK, Brown CA, Xia H, Xu J, et al. (2012) No Differential Regulation of Dopamine Transporter (DAT) and Vesicular Monoamine Transporter 2 (VMAT2) Binding in a Primate Model of Parkinson Disease. PLoS One 7: e31439. doi: 10.1371/journal.pone.0031439 PMID: 22359591
10. Tabbal SD, Tian L, Karimi M, Brown CA, Loftin SK, Perlmutter JS (2012) Low nigrostriatal reserve for motor parkinsonism in nonhuman primates. Exp Neurol 237: 355-362. S0014-4886(12)00285-3 [pii]; doi: 10.1016/j.expneurol.2012.07.008 PMID: 22836146
11. Karimi M, Tian L, Brown CA, Flores HP, Loftin SK, Videen TO, et al. (2013) Validation of nigrostriatal positron emission tomography measures: Critical limits. Ann Neurol 73: 390-396. doi: 10.1002/ana.23798 PMID: 23423933
12. Tian L, Karimi M, Brown CA, Loftin SK, Perlmutter JS (2014) In vivo measures of nigrostriatal neuronal response to unilateral MPTP treatment. Brain Res 1571: 49-60. S0006-8993(14)00678-7 [pii]; doi: 10.1016/j.brainres.2014.05.009 PMID: 24845719
13. Starkstein SE, Leentjens AF (2008) The nosological position of apathy in clinical practice. J Neurol Neurosurg Psychiatry 79: 1088-1092. jnnp.2007.136895 [pii]; doi: 10.1136/jnnp.2007.136895 PMID: 18187477
14. Perlmutter JS, Tempel LW, Black KJ, Parkinson D, Todd RD (1997) MPTP induces dystonia and parkinsonism. Clues to the pathophysiology of dystonia. Neurology 49: 1432-1438. PMID: 9371934
15. Rowland DJ, Garbow JR, Laforest R, Snyder AZ (2005) Registration of [18F]FDG microPET and small-animal MRI. Nucl Med Biol 32: 567-572. S0969-8051(05)00125-3 [pii]; doi: 10.1016/j.nucmedbio.2005.05.002 PMID: 16026703
16. Crespo-Facorro B, Kim JJ, Andreasen NC, O'Leary DS, Wiser AK, Bailey JM, et al. (1999) Human frontal cortex: an MRI-based parcellation method. Neuroimage 10: 500-519. doi: 10.1006/nimg.1999.0489;S1053-8119(99)90489-5 [pii]. PMID: 10547328
17. Saleem Kadharbatcha S. and Logothetis Nikos K. (2012) A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates. Academic Press.
18. Pengas G, Hodges JR, Watson P, Nestor PJ (2010) Focal posterior cingulate atrophy in incipient Alzheimer's disease. Neurobiol Aging 31: 25-33. S0197-4580(08)00103-6 [pii]; doi: 10.1016/j.neurobiolaging.2008.03.014 PMID: 18455838
19. Takahashi T, Suzuki M, Hagino H, Zhou SY, Kawasaki Y, Nohara S, et al. (2004) Bilateral volume reduction of the insular cortex in patients with schizophrenia: a volumetric MRI Study. Psychiatry Res 132: 187-196. PMID: 15658005
20. Logan J (2000) Graphical analysis of PET data applied to reversible and irreversible tracers. Nucl Med Biol 27: 661-670. S0969-8051(00)00137-2 [pii]. PMID: 11091109
21. Patlak CS, Blasberg RG (1985) Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J Cereb Blood Flow Metab 5: 584-590. doi: 10.1038/jcbfm.1985.87 PMID: 4055928
22. Patlak CS, Blasberg RG, Fenstermacher JD (1983) Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J Cereb Blood Flow Metab 3: 1-7. doi: 10.1038/jcbfm.1983.1 PMID: 6822610
23. Sossi V, Holden JE, Chan G, Krzywinski M, Stoessl AJ, Ruth TJ (2000) Analysis of four dopaminergic tracers kinetics using two different tissue input function methods. J Cereb Blood Flow Metab 20: 653-660. doi: 10.1097/00004647-200004000-00002 PMID: 10779009
24. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, et al. (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96: 379-394. PMID: 3288247
25. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, et al. (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96: 857-881. PMID: 3056461
26. Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. Brain 118 (Pt 4): 913-933. PMID: 7655888
27. Damasio Antonio (2008) Descartes' error: Emotion, reason and the human brain. Random House.
28. Manes F, Paradiso S, Robinson RG (1999) Neuropsychiatric effects of insular stroke. J Nerv Ment Dis 187: 707-712. PMID: 10665464
29. Migneco O, Benoit M, Koulibaly PM, Dygai I, Bertogliati C, Desvignes P, et al. (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. Neuroimage 13: 896-902. doi: 10.1006/nimg.2000.0741;S1053-8119(00)90741-9 [pii]. PMID: 11304085
30. Craig AH, Cummings JL, Fairbanks L, Itti L, Miller BL, Li J, et al. (1996) Cerebral blood flow correlates of apathy in Alzheimer disease. Arch Neurol 53: 1116-1120. PMID: 8912484
31. Le JF, Drapier D, Bourguignon A, Peron J, Mesbah H, Drapier S, et al. (2009) Subthalamic nucleus stimulation in Parkinson disease induces apathy: a PET study. Neurology 73: 1746-1751. 73/21/1746 [pii]; doi: 10.1212/WNL.0b013e3181c34b34 PMID: 19933975
32. Braak H, Braak E (1995) Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiology of aging 16: 271-278. PMID: 7566337
33. Ohara PT, Granato A, Moallem TM, Wang BR, Tillet Y, Jasmin L (2003) Dopaminergic input to GABAergic neurons in the rostral agranular insular cortex of the rat. J Neurocytol 32: 131-141. 5146661 [pii]. PMID: 14707548
34. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, et al. (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27: 2349-2356. 27/9/2349 [pii]; doi: 10.1523/JNEUROSCI.5587-06.2007 PMID: 17329432
35. Ongur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10: 206-219. PMID: 10731217
36. Oades RD, Halliday GM (1987) Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 434: 117-165. PMID: 3107759
37. Nieuwenhuys R (2011) The insular cortex: a review. Progress in brain research 195: 123-163.
38. Mutschler I, Wieckhorst B, Kowalevski S, Derix J, Wentlandt J, Schulze-Bonhage A, et al. (2009) Functional organization of the human anterior insular cortex. Neurosci Lett 457: 66-70. S0304-3940(09)00422-4 [pii]; doi: 10.1016/j.neulet.2009.03.101 PMID: 19429164
39. Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214: 519-534. doi: 10.1007/s00429-010-0255-z PMID: 20512376
40. Fasold O, von BM, Kuhberg M, Ploner CJ, Villringer A, Lempert T, et al. (2002) Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. Neuroimage 17: 1384-1393. S1053811902912413 [pii]. PMID: 12414278
41. Brandt T, Dieterich M (1999) The vestibular cortex. Its locations, functions, and disorders. Ann N Y Acad Sci 871: 293-312. PMID: 10372080
42. Brandt T, Dieterich M, Danek A (1994) Vestibular cortex lesions affect the perception of verticality. Ann Neurol 35: 403-412. doi: 10.1002/ana.410350406 PMID: 8154866
43. Agid Y, Javoy-Agid F, Ruberg M (1987) Biochemistry of neurotransmitters in Parkinson's disease. Movement disorders 2: 166-230.
44. Gibb WR, Lees AJ (1991) Anatomy, pigmentation, ventral and dorsal subpopulations of the substantia nigra, and differential cell death in Parkinson's disease. J Neurol Neurosurg Psychiatry 54: 388-396. PMID: 1865199
45. Perez-Otano I, Oset C, Luquin MR, Herrero MT, Obeso JA, Del RJ (1994) MPTP-induced parkinsonism in primates: pattern of striatal dopamine loss following acute and chronic administration. Neurosci Lett 175: 121-125. PMID: 7970192
46. Burns RS, Chiueh CC, Markey SP, Ebert MH, Jacobowitz DM, Kopin IJ (1983) A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc Natl Acad Sci U S A 80: 4546-4550. PMID: 6192438
47. Hallman H, Olson L, Jonsson G (1984) Neurotoxicity of the meperidine analogue N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on brain catecholamine neurons in the mouse. Eur J Pharmacol 97: 133-136. PMID: 6607840
48. Wallace RA, Boldry R, Schmittgen T, Miller D, Uretsky N (1984) Effect of 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine (MPTP) on monoamine neurotransmitters in mouse brain & heart. Life Sci 35: 285-291. PMID: 6146909
49. Barnhart WJ, Makela EH, Latocha MJ (2004) SSRI-induced apathy syndrome: a clinical review. J Psychiatr Pract 10: 196-199. 00131746-200405000-00010 [pii]. PMID: 15330228
50. McKeith I, Del ST, Spano P, Emre M, Wesnes K, Anand R, et al. (2000) Efficacy of rivastigmine in dementia with Lewy bodies: a randomised, double-blind, placebo-controlled international study. Lancet 356: 2031-2036. S0140-6736(00)03399-7 [pii]; doi: 10.1016/S0140-6736(00)03399-7 PMID:11145488