Thalamic degeneration in MPTP-treated Parkinsonian monkeys: impact upon glutamatergic innervation of striatal cholinergic interneurons.

Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 101282001 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1863-2661 (Electronic) Linking ISSN: 18632653 NLM ISO Abbreviation: Brain Struct Funct Subsets: MEDLINE

Original Publication: Berlin : Springer-Verlag, c2007-

Glutamic Acid*; Caudate Nucleus/*pathology ; Cholinergic Neurons/*pathology ; Intralaminar Thalamic Nuclei/*pathology ; Neurons/*pathology ; Parkinsonian Disorders/*pathology ; Putamen/*pathology; Animals ; Caudate Nucleus/ultrastructure ; Cholinergic Neurons/ultrastructure ; Female ; Interneurons/pathology ; Interneurons/ultrastructure ; Intralaminar Thalamic Nuclei/ultrastructure ; Macaca mulatta ; Male ; Neural Pathways/pathology ; Neural Pathways/ultrastructure ; Neurons/ultrastructure ; Putamen/ultrastructure ; Synapses/pathology ; Synapses/ultrastructure ; Vesicular Glutamate Transport Protein 2/metabolism

In both Parkinson's disease (PD) patients and MPTP-treated non-human primates, there is a profound neuronal degeneration of the intralaminar centromedian/parafascicular (CM/Pf) thalamic complex. Although this thalamic pathology has long been established in PD (and other neurodegenerative disorders), the impact of CM/Pf cell loss on the integrity of the thalamo-striatal glutamatergic system and its regulatory functions upon striatal neurons remain unknown. In the striatum, cholinergic interneurons (ChIs) are important constituents of the striatal microcircuitry and represent one of the main targets of CM/Pf-striatal projections. Using light and electron microscopy approaches, we have analyzed the potential impact of CM/Pf neuronal loss on the anatomy of the synaptic connections between thalamic terminals (vGluT2-positive) and ChIs neurons in the striatum of parkinsonian monkeys treated chronically with MPTP. The following conclusions can be drawn from our observations: (1) as reported in PD patients, and in our previous monkey study, CM/Pf neurons undergo profound degeneration in monkeys chronically treated with low doses of MPTP. (2) In the caudate (head and body) nucleus of parkinsonian monkeys, there is an increased density of ChIs. (3) Despite the robust loss of CM/Pf neurons, no significant change was found in the density of thalamostriatal (vGluT2-positive) terminals, and in the prevalence of vGluT2-positive terminals in contact with ChIs in parkinsonian monkeys. These findings provide new information about the state of thalamic innervation of the striatum in parkinsonian monkeys with CM/Pf degeneration, and bring up an additional level of intricacy to the consequences of thalamic pathology upon the functional microcircuitry of the thalamostriatal system in parkinsonism. Future studies are needed to assess the importance of CM/Pf neuronal loss, and its potential consequences on the neuroplastic changes induced in the synaptic organization of the thalamostriatal system, in the development of early cognitive impairments in PD.

Brain. 2011 Jul;134(Pt 7):2057-73. (PMID: 21705423)
Eur J Neurosci. 2002 Jun;15(12):1918-28. (PMID: 12099898)
Science. 1990 Dec 7;250(4986):1429-32. (PMID: 2147780)
Learn Mem. 2013 Sep 18;20(10):592-600. (PMID: 24049188)
Neuroscience. 2005;136(4):1083-95. (PMID: 16226840)
Eur J Neurosci. 2019 Mar;49(5):593-603. (PMID: 29480942)
Eur J Pharmacol. 1986 Nov 19;131(2-3):199-209. (PMID: 3493157)
J Comp Neurol. 2013 Aug 1;521(11):2502-22. (PMID: 23296794)
Neuron. 2004 Jul 8;43(1):133-43. (PMID: 15233923)
J Comp Neurol. 1992 Jan 8;315(2):137-59. (PMID: 1372010)
Front Neuroanat. 2014 Dec 03;8:146. (PMID: 25520629)
J Neurosci. 2011 Jan 26;31(4):1507-15. (PMID: 21273435)
Brain. 2015 Apr;138(Pt 4):946-62. (PMID: 25681412)
Neurosci Res. 2004 Apr;48(4):355-60. (PMID: 15041188)
Front Neuroanat. 2010 Nov 01;4:138. (PMID: 21088699)
Front Neural Circuits. 2013 Jan 24;7:2. (PMID: 23355811)
Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21848-53. (PMID: 21115815)
Prog Neuropsychopharmacol Biol Psychiatry. 2001 Jan;25(1):211-30. (PMID: 11263753)
Eur J Neurosci. 2008 Apr;27(7):1647-58. (PMID: 18380666)
Mov Disord. 2011 Jan;26(1):6-17. (PMID: 21322014)
Prog Brain Res. 2007;160:313-29. (PMID: 17499122)
Restor Neurol Neurosci. 2000;16(2):135-142. (PMID: 12671216)
J Microsc. 1998 Nov;192(Pt 2):163-71. (PMID: 9853373)
Mov Disord. 2014 Apr;29(4):508-17. (PMID: 24515328)
Curr Opin Neurobiol. 2018 Feb;48:9-16. (PMID: 28843800)
Cell Rep. 2015 Oct 27;13(4):657-666. (PMID: 26489458)
Neuron. 2019 Feb 6;101(3):444-458.e6. (PMID: 30658860)
J Neurophysiol. 1999 Feb;81(2):858-74. (PMID: 10036286)
Neuroscience. 1999;89(4):1189-208. (PMID: 10362307)
Trends Neurosci. 1995 Dec;18(12):527-35. (PMID: 8638293)
J Chem Neuroanat. 2000 Jul;19(3):155-73. (PMID: 10989260)
Trends Neurosci. 1999 Feb;22(2):51-61. (PMID: 10092043)
NPJ Parkinsons Dis. 2018 Aug 2;4:23. (PMID: 30083593)
Brain Res. 2009 May 19;1271:83-94. (PMID: 19328193)
Curr Biol. 2016 Feb 22;26(4):550-5. (PMID: 26877079)
Brain Res. 2015 Dec 2;1628(Pt A):104-16. (PMID: 25514336)
J Neurosci Res. 2015 Aug;93(8):1184-91. (PMID: 25914366)
J Neural Transm (Vienna). 2018 Mar;125(3):501-513. (PMID: 28324169)
Prog Brain Res. 1993;99:25-34. (PMID: 8108552)
J Comp Neurol. 1987 Jan 8;255(2):245-58. (PMID: 3819015)
Brain Struct Funct. 2019 Dec;224(9):3321-3338. (PMID: 31679085)
Mol Neurobiol. 2013 Feb;47(1):117-22. (PMID: 22923348)
Mov Disord. 2009 Oct 30;24(14):2128-35. (PMID: 19735086)
Neurobiol Dis. 2016 Nov;95:46-53. (PMID: 27388937)
Neurobiol Dis. 2016 Jul;91:47-58. (PMID: 26921469)
Basal Ganglia. 2011 Nov 1;1(4):179-189. (PMID: 22773963)
Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3413-8. (PMID: 15716361)
Geriatr Gerontol Int. 2010 Jul;10 Suppl 1:S148-57. (PMID: 20590830)
Trends Neurosci. 2004 Sep;27(9):520-7. (PMID: 15331233)
Neurosci Res. 1996 Aug;25(4):309-34. (PMID: 8866512)
J Neurosci. 2010 Oct 27;30(43):14390-8. (PMID: 20980596)
J Microsc. 1986 Jul;143(Pt 1):3-45. (PMID: 3761363)
Eur J Neurosci. 2019 Mar;49(5):658-671. (PMID: 29791051)
Psychopharmacology (Berl). 2017 Aug;234(16):2399-2407. (PMID: 28451710)
Eur J Neurosci. 2009 Feb;29(3):588-98. (PMID: 19175404)
Front Neuroanat. 2011 Feb 07;5:6. (PMID: 21344017)
Neuroscience. 1991;40(1):133-58. (PMID: 2052148)
Neuroscience. 2005;130(4):813-31. (PMID: 15652981)
J Neurosci. 2014 Feb 19;34(8):3090-4. (PMID: 24553948)
J Neural Transm (Vienna). 2018 Mar;125(3):279-290. (PMID: 28168621)
Behav Brain Res. 2005 Jul 30;162(2):222-32. (PMID: 15970217)
Eur J Neurosci. 2018 May;47(10):1148-1158. (PMID: 28677242)
J Neurosci. 2003 Sep 17;23(24):8489-97. (PMID: 13679417)
Brain Res. 1997 Jun 6;759(1):9-17. (PMID: 9219857)
Brain Res Bull. 2009 Feb 16;78(2-3):60-8. (PMID: 18805468)
Brain Res. 1990 Jun 11;519(1-2):122-8. (PMID: 2397401)
Neurobiol Learn Mem. 2014 Feb;108:104-18. (PMID: 24231424)
Exp Neurol. 2010 Dec;226(2):265-73. (PMID: 20832405)
Neuroscience. 1984 Jul;12(3):669-86. (PMID: 6382047)
J Comp Neurol. 2006 Nov 10;499(2):231-43. (PMID: 16977615)
Brain Res Bull. 2009 Feb 16;78(2-3):97-104. (PMID: 18804518)
J Neural Transm (Vienna). 2018 Mar;125(3):337-363. (PMID: 28861737)
J Neurophysiol. 2002 Jun;87(6):3090-101. (PMID: 12037210)
Ann Neurol. 2000 Mar;47(3):345-52. (PMID: 10716254)
J Mol Neurosci. 1995;6(4):225-35. (PMID: 8860234)
Brain Struct Funct. 2014 Jan;219(1):381-94. (PMID: 23508713)
Eur J Neurosci. 2019 Mar;49(5):604-622. (PMID: 29797362)
Toxicology. 1988 Apr;49(1):17-23. (PMID: 3287690)
J Comp Neurol. 2005 Jan 3;481(1):127-44. (PMID: 15558721)
J Microsc. 1981 Jan;121(Pt 1):65-73. (PMID: 7014910)
Parkinsonism Relat Disord. 2009 Dec;15 Suppl 3:S152-5. (PMID: 20082979)
Ann N Y Acad Sci. 2005 May;1041:510-5. (PMID: 15956753)
J Neurosci. 2015 Jun 17;35(24):8979-85. (PMID: 26085623)
PLoS One. 2007 Nov 14;2(11):e1174. (PMID: 18080007)
PLoS One. 2012;7(1):e30504. (PMID: 22272358)
J Neurosci. 2008 Nov 5;28(45):11673-84. (PMID: 18987203)
Brain. 2000 Jul;123 ( Pt 7):1410-21. (PMID: 10869053)
Eur J Neurosci. 2006 Apr;23(8):2099-108. (PMID: 16630057)
Neuron. 2016 Feb 17;89(4):734-40. (PMID: 26833136)
Neurobiol Dis. 2013 Dec;60:89-107. (PMID: 23969239)
Neuron. 2016 Apr 20;90(2):362-73. (PMID: 27100198)
J Comp Neurol. 1990 Sep 8;299(2):187-228. (PMID: 2172326)
Neurotoxicology. 1991 Summer;12(2):285-302. (PMID: 1956587)
Ann N Y Acad Sci. 2015 Sep;1349:1-45. (PMID: 25876458)
Front Neuroanat. 2015 Sep 25;9:117. (PMID: 26441550)
Nat Rev Neurosci. 2014 Jan;15(1):63. (PMID: 24301065)
J Neurosci. 2019 Jan 2;39(1):3-14. (PMID: 30389839)
Neuron. 2013 Jul 10;79(1):153-66. (PMID: 23770257)
Pharmacol Ther. 2014 Oct;144(1):50-9. (PMID: 24836728)
Neuroscience. 2013 Oct 22;251:2-20. (PMID: 23867772)
J Comp Neurol. 2011 Apr 1;519(5):989-1005. (PMID: 21280048)
J Neuropathol Exp Neurol. 2004 Jan;63(1):20-31. (PMID: 14748558)
J Neurosci. 2017 Mar 29;37(13):3721-3733. (PMID: 28242795)
J Neurosci. 2008 May 28;28(22):5641-53. (PMID: 18509025)
J Neural Transm (Vienna). 2018 Mar;125(3):431-447. (PMID: 28540422)
Am J Psychiatry. 2007 Oct;164(10):1603-9; quiz 1624. (PMID: 17898353)
Cold Spring Harb Perspect Med. 2012 Dec 01;2(12):a009621. (PMID: 23071379)
Prog Brain Res. 1993;99:227-35. (PMID: 8108550)
J Comp Neurol. 1990 Jun 8;296(2):204-21. (PMID: 2358532)
Brain. 2005 Oct;128(Pt 10):2272-80. (PMID: 16014651)
J Comp Neurol. 1996 Mar 18;366(4):580-99. (PMID: 8833111)
Front Neuroanat. 2010 Dec 10;4:133. (PMID: 21179580)
J Neurosci. 1994 Jun;14(6):3969-84. (PMID: 8207500)
Neuroscience. 1986 Jun;18(2):347-71. (PMID: 3736862)
Brain Res Mol Brain Res. 1992 Apr;13(3):251-61. (PMID: 1317497)
J Neurosci. 2011 Nov 9;31(45):16102-6. (PMID: 22072662)
Neurochem Res. 2019 May;44(5):1079-1089. (PMID: 30715657)
Brain Res. 2012 Mar 29;1446:46-55. (PMID: 22353754)
PLoS One. 2015 Apr 01;10(4):e0123381. (PMID: 25830919)
Neuron. 2001 Aug 2;31(2):247-60. (PMID: 11502256)
Neuropharmacology. 2003 Jul;45(1):45-56. (PMID: 12814658)
J Comp Neurol. 2010 Jul 1;518(13):2525-37. (PMID: 20503425)
Med Sci Monit. 2005 Jan;11(1):RA17-23. (PMID: 15614202)
Neuroscience. 1992 Dec;51(3):533-45. (PMID: 1488113)
Neuroscience. 2002;115(2):533-46. (PMID: 12421620)
Front Syst Neurosci. 2014 Jan 30;8:5. (PMID: 24523677)
Curr Opin Neurobiol. 2004 Dec;14(6):685-92. (PMID: 15582369)
J Comp Neurol. 1992 Jun 8;320(2):228-42. (PMID: 1619051)
Brain. 2003 Jun;126(Pt 6):1392-408. (PMID: 12764060)
Trends Neurosci. 2007 Oct;30(10):545-53. (PMID: 17904652)
Nature. 1990 Mar 15;344(6263):240-2. (PMID: 2314459)
Neuron. 2010 Jul 29;67(2):294-307. (PMID: 20670836)
Proc Natl Acad Sci U S A. 2011 Jan 11;108(2):840-5. (PMID: 21187382)
J Neurosci. 2007 Aug 1;27(31):8161-5. (PMID: 17670959)
Neuroscience. 1996 Nov;75(2):523-33. (PMID: 8931015)
Front Syst Neurosci. 2014 May 09;8:83. (PMID: 24847225)
Neurology. 2010 Oct 5;75(14):1263-9. (PMID: 20810998)
Behav Brain Res. 2016 Feb 1;298(Pt B):192-201. (PMID: 26393431)

R01 NS083386 United States NS NINDS NIH HHS; P51 OD011132 United States OD NIH HHS; RO1NS083386 Foundation for the National Institutes of Health (US); P50NS098685 United States NH NIH HHS; P50 NS098685 United States NS NINDS NIH HHS; P51OD011132 NIH/ORIP

Keywords: Non-human primates; Parafascicular; Parkinson’s disease; Striatum; Thalamostriatal; vGluT2

0 (Vesicular Glutamate Transport Protein 2)
3KX376GY7L (Glutamic Acid)

Date Created: 20191104 Date Completed: 20200414 Latest Revision: 20231020

20240829

PMC6878768

10.1007/s00429-019-01967-w

31679085