Brain networks in Huntington disease

Journal of Clinical Investigation

Volumn 121, Issue 2, 2011, Pages 484-492

  Eidelberg, David ^a   Surmeier, D James ^b  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DOPAMINE 2 RECEPTOR; HUNTINGTIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

BRAIN CORTEX; BRAIN DYSFUNCTION; BRAIN METABOLISM; BRAIN NERVE CELL; BRAIN REGION; CEREBELLUM; CORPUS STRIATUM; DISEASE COURSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOBUS PALLIDUS; HOMEOSTASIS; HUMAN; HUNTINGTON CHOREA; HYPOTHALAMUS; INTRACELLULAR SIGNALING; NERVE CELL NETWORK; NEUROPATHOLOGY; NONHUMAN; PATHOGENESIS; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SPINY PROJECTION NEURON; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS; THALAMUS;

ANIMALS; CEREBRAL CORTEX; DIAGNOSTIC IMAGING; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HOMEOSTASIS; HUMANS; HUNTINGTON DISEASE; NERVE NET;

EID: 79551519277     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45646     Document Type: Review

References (115)

1. Zuccato C, Valenza M, Cattaneo E. Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol Rev. 2010;90(3):905-981.
2. Sapp E, et al. Huntingtin localization in brains of normal and Huntington's disease patients. Ann Neurol. 1997;42(4):604-612.
3. Fusco FR, et al. Cellular localization of huntingtin in striatal and cortical neurons in rats: lack of correlation with neuronal vulnerability in Huntington's disease. J Neurosci. 1999;19(4):1189-1202.
4. Reiner A, Albin RL, Anderson KD, D'Amato CJ, Penney JB, Young AB. Differential loss of striatal projection neurons in Huntington disease. Proc Natl Acad Sci U S A. 1988;85(15):5733-5737.
5. Vonsattel JP, DiFiglia M. Huntington disease. J Neuropathol Exp Neurol. 1998;57(5):369-384.
6. Balleine BW, Liljeholm M, Ostlund SB. The integrative function of the basal ganglia in instrumental conditioning. Behav Brain Res. 2009;199(1):43-52.
7. Gerfen CR, et al. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science. 1990;250(4986):1429-1432.
8. Surmeier DJ, Song WJ, Yan Z. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci. 1996;16(20):6579-6591. (Pubitemid 26337379)
9. Gertler TS, Chan CS, Surmeier DJ. Dichotomous anatomical properties of adult striatal medium spiny neurons. J Neurosci. 2008;28(43):10814-10824.
10. Surmeier DJ, Ding J, Day M, Wang Z, Shen W. D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci. 2007;30(5):228-235.
11. Bolam JP, Hanley JJ, Booth PA, Bevan MD. Synaptic organisation of the basal ganglia. J Anat. 2000;196(pt 4):527-542.
12. Doig NM, Moss J, Bolam JP. Cortical and thalamic innervation of direct and indirect pathway medium-sized spiny neurons in mouse striatum. J Neurosci. 2010;30(44):14610-14618.
13. Kravitz AV, et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature. 2010;466(7306):622-626.
14. Albin RL, et al. Abnormalities of striatal projection neurons and N-methyl-D-aspartate receptors in presymptomatic Huntington's disease. N Engl J Med. 1990;322(18):1293-1298.
15. Sapp E, et al. Evidence for a preferential loss of enkephalin immunoreactivity in the external globus pallidus in low grade Huntington's disease using high resolution image analysis. Neuroscience. 1995;64(2):397-404.
16. Leavitt BR, Hayden MR. Is tetrabenazine safe and effective for suppressing chorea in Huntington's disease? Nat Clin Pract Neurol. 2006;2(10):536-537.
17. Guay DR. Tetrabenazine, a monoamine-depleting drug used in the treatment of hyperkinetic movement disorders. Am J Geriatr Pharmacother. 2010;8(4):331-373.
18. Grimbergen YA, Roos RA. Therapeutic options for Huntington's disease. Curr Opin Investig Drugs. 2003;4(1):51-54.
19. Surmeier DJ, et al. The role of dopamine in modulating the structure and function of striatal circuits. Prog Brain Res. 2010;183:149-167.
20. Thu DC, et al. Cell loss in the motor and cingulate cortex correlates with symptomatology in Huntington's disease. Brain. 2010;133(pt 4):1094-1110.
21. Heinsen H, et al. Nerve cell loss in the thalamic centromedian- parafascicular complex in patients with Huntington's disease. Acta Neuropathol. 1996;91(2):161-168.
22. Heinsen H, et al. Nerve cell loss in the thalamic mediodorsal nucleus in Huntington's disease. Acta Neuropathol. 1999;97(6):613-622.
23. Petersen A, Bjorkqvist M. Hypothalamic-endocrine aspects in Huntington's disease. Eur J Neurosci. 2006;24(4):961-967.
24. Gabery S, et al. Changes in key hypothalamic neuropeptide populations in Huntington disease revealed by neuropathological analyses. Acta Neuropathol. 2010;120(6):777-788.
25. Rosas HD, et al. Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology. 2003;60(10):1615-1620.
26. Milnerwood AJ, Raymond LA. Early synaptic pathophysiology in neurodegeneration: insights from Huntington's disease. Trends Neurosci. 2010;33(11):513-523.
27. Zuccato C, Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol. 2009;5(6):311-322.
28. Zuccato C, Marullo M, Conforti P, MacDonald ME, Tartari M, Cattaneo E. Systematic assessment of BDNF and its receptor levels in human cortices affected by Huntington's disease. Brain Pathol. 2008;18(2):225-238.
29. Zuccato C, et al. Progressive loss of BDNF in a mouse model of Huntington's disease and rescue by BDNF delivery. Pharmacol Res. 2005;52(2):133-139. (Pubitemid 40828363)
30. Zuccato C, et al. Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science. 2001;293(5529):493-498. (Pubitemid 32679077)
31. Strand AD, et al. Expression profiling of Huntington's disease models suggests that brain-derived neurotrophic factor depletion plays a major role in striatal degeneration. J Neurosci. 2007;27(43):11758-11768.
32. Canals JM, et al. Brain-derived neurotrophic factor regulates the onset and severity of motor dysfunction associated with enkephalinergic neuronal degeneration in Huntington's disease. J Neurosci. 2004;24(35):7727-7739.
33. Gharami K, Xie Y, An JJ, Tonegawa S, Xu B. Brain-derived neurotrophic factor over-expression in the forebrain ameliorates Huntington's disease phenotypes in mice. J Neurochem. 2008;105(2):369-379. (Pubitemid 351490006)
34. Xie H, et al. Brain-derived neurotrophic factor rescues and prevents chronic intermittent hypoxia-induced impairment of hippocampal long-term synaptic plasticity. Neurobiol Dis. 2010;40(1):155-162.
35. Gauthier LR, et al. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell. 2004;118(1):127-138.
36. Her LS, Goldstein LS. Enhanced sensitivity of striatal neurons to axonal transport defects induced by mutant huntingtin. J Neurosci. 2008;28(50):13662- 13672.
37. Gu X, et al. Pathological cell-cell interactions are necessary for striatal pathogenesis in a conditional mouse model of Huntington's disease. Mol Neurodegener. 2007;2:8.
38. Baquet ZC, Gorski JA, Jones KR. Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J Neurosci. 2004;24(17):4250-4258.
39. Kang H, Schuman EM. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 1995;267(5204):1658- 1662.
40. Lu Y, Christian K, Lu B. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem. 2008;89(3):312-323.
41. Lobo MK, et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science. 2010;330(6002):385-390.
42. Jia Y, Gall CM, Lynch G. Presynaptic BDNF promotes postsynaptic long-term potentiation in the dorsal striatum. J Neurosci. 2010;30(43):14440-14445.
43. Kung VW, Hassam R, Morton AJ, Jones S. Dopamine-dependent long term potentiation in the dorsal striatum is reduced in the R6/2 mouse model of Huntington's disease. Neuroscience. 2007;146(4):1571-1580.
44. Picconi B, et al. Plastic and behavioral abnormalities in experimental Huntington's disease: a crucial role for cholinergic interneurons. Neurobiol Dis. 2006;22(1):143-152.
45. Usdin MT, Shelbourne PF, Myers RM, Madison DV. Impaired synaptic plasticity in mice carrying the Huntington's disease mutation. Hum Mol Genet. 1999;8(5):839-846.
46. Lynch G, et al. Brain-derived neurotrophic factor restores synaptic plasticity in a knock-in mouse model of Huntington's disease. J Neurosci. 2007;27(16):4424-4434.
47. Wang H, Chen X, Li Y, Tang TS, Bezprozvanny I. Tetrabenazine is neuroprotective in Huntington's disease mice. Mol Neurodegener. 2010;5:18.
48. Cyr M, Sotnikova TD, Gainetdinov RR, Caron MG. Dopamine enhances motor and neuropathological consequences of polyglutamine expanded huntingtin. FASEB J. 2006;20(14):2541-2543.
49. Glass M, Dragunow M, Faull RL. The pattern of neurodegeneration in Huntington's disease: a comparative study of cannabinoid, dopamine, adenosine and GABA(A) receptor alterations in the human basal ganglia in Huntington's disease. Neuroscience. 2000;97(3):505-519.
50. Denovan-Wright EM, Robertson HA. Cannabinoid receptor messenger RNA levels decrease in a subset of neurons of the lateral striatum, cortex and hippocampus of transgenic Huntington's disease mice. Neuroscience. 2000;98(4):705-713.
51. McCaw EA, Hu H, Gomez GT, Hebb AL, Kelly ME, Denovan-Wright EM. Structure, expression and regulation of the cannabinoid receptor gene (CB1) in Huntington's disease transgenic mice. Eur J Biochem. 2004;271(23-24):4909-4920.
52. Lastres-Becker I, Gomez M, De Miguel R, Ramos JA, Fernandez-Ruiz J. Loss of cannabinoid CB(1) receptors in the basal ganglia in the late akinetic phase of rats with experimental Huntington's disease. Neurotox Res. 2002;4(7-8):601-608.
53. Lovinger DM. Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology. 2010;58(7):951-961.
54. Cepeda C, Cummings DM, Andre VM, Holley SM, Levine MS. Genetic mouse models of Huntington's disease: focus on electrophysiological mechanisms. ASN Neuro. 2010;2(2):e00033.
55. Milnerwood AJ, et al. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron. 2010;65(2):178-190.
56. Okamoto S, et al. Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat Med. 2009;15(12):1407-1413.
57. Hansson O, et al. Resistance to NMDA toxicity correlates with appearance of nuclear inclusions, behavioural deficits and changes in calcium homeostasis in mice transgenic for exon 1 of the huntington gene. Eur J Neurosci. 2001;14(9):1492-1504.
58. Petersen A, Chase K, Puschban Z, DiFiglia M, Brundin P, Aronin N. Maintenance of susceptibility to neurodegeneration following intrastriatal injections of quinolinic acid in a new transgenic mouse model of Huntington's disease. Exp Neurol. 2002;175(1):297-300.
59. Cowan CM, et al. Polyglutamine-modulated striatal calpain activity in YAC transgenic huntington disease mouse model: impact on NMDA receptor function and toxicity. J Neurosci. 2008;28(48):12725-12735.
60. Prybylowski K, Chang K, Sans N, Kan L, Vicini S, Wenthold RJ. The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron. 2005;47(6):845-857.
61. Wu HY, Hsu FC, Gleichman AJ, Baconguis I, Coulter DA, Lynch DR. Fyn-mediated phosphorylation of NR2B Tyr-1336 controls calpain-mediated NR2B cleavage in neurons and heterologous systems. J Biol Chem. 2007;282(28):20075- 20087.
62. Wilson CJ, Kawaguchi Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci. 1996;16(7):2397-2410.
63. Tang TS, et al. Disturbed Ca2+ signaling and apoptosis of medium spiny neurons in Huntington's disease. Proc Natl Acad Sci U S A. 2005;102(7):2602- 2607.
64. Tang TS, Chen X, Liu J, Bezprozvanny I. Dopaminergic signaling and striatal neurodegeneration in Huntington's disease. J Neurosci. 2007;27(30):7899-7910.
65. Beal MF. Huntington's disease, energy, and excitotoxicity. Neurobiol Aging. 1994;15(2):275-276.
66. Schwarcz R, Guidetti P, Sathyasaikumar KV, Muchowski PJ. Of mice, rats and men: Revisiting the quinolinic acid hypothesis of Huntington's disease. Prog Neurobiol. 2010;90(2):230-245.
67. Turrigiano G. Homeostatic signaling: the positive side of negative feedback. Curr Opin Neurobiol. 2007;17(3):318-324.
68. Day M, et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci. 2006;9(2):251-259.
69. Warre R, et al. Altered function of glutamatergic cortico-striatal synapses causes output pathway abnormalities in a chronic model of parkinsonism [published online ahead of print October 21, 2010]. Neurobiol Dis. doi:10.1016/j.nbd.2010.10.013.
70. Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ. Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 2002;25(10):525-531.
71. Chan CS, et al. HCN channelopathy in external globus pallidus neurons in models of Parkinson's disease. Nat Neurosci. 2011;14(1):85-92.
72. Mallet N, et al. Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex. J Neurosci. 2008;28(18):4795-4806.
73. Tang JK, et al. Firing rates of pallidal neurons are similar in Huntington's and Parkinson's disease patients. Exp Brain Res. 2005;166(2):230-236.
74. Starr PA, Kang GA, Heath S, Shimamoto S, Turner RS. Pallidal neuronal discharge in Huntington's disease: support for selective loss of striatal cells originating the indirect pathway. Exp Neurol. 2008;211(1):227-233.
75. Fasano A, Mazzone P, Piano C, Quaranta D, Soleti F, Bentivoglio AR. GPi-DBS in Huntington's disease: results on motor function and cognition in a 72-year-old case. Mov Disord. 2008;23(9):1289-1292.
76. Paulsen JS. Functional imaging in Huntington's disease. Exp Neurol. 2009;216(2):272-277.
77. Esmaeilzadeh M, Ciarmiello A, Squitieri F. Seeking brain biomarkers for preventive therapy in Huntington disease [published online ahead of print June 11, 2010]. CNS Neurosci Ther. doi:10.1111/j.1755-5949.2010.00157.x.
78. Jenkins BG, et al. Effects of CAG repeat length, HTT protein length and protein context on cerebral metabolism measured using magnetic resonance spectroscopy in transgenic mouse models of Huntington's disease. J Neurochem. 2005;95(2):553-562.
79. Rosas HD, Salat DH, Lee SY, Zaleta AK, Hevelone N, Hersch SM. Complexity and heterogeneity: what drives the ever-changing brain in Huntington's disease? Ann N Y Acad Sci. 2008;1147:196-205.
80. Montoya A, Price BH, Menear M, Lepage M. Brain imaging and cognitive dysfunctions in Huntington's disease. J Psychiatry Neurosci. 2006;31(1):21-29.
81. Kuwert T, Lange HW, Langen KJ, Herzog H, Aulich A, Feinendegen LE. Cortical and subcortical glucose consumption measured by PET in patients with Huntington's disease. Brain. 1990;113(pt 5):1405-1423.
82. Cha JH, et al. Altered neurotransmitter receptor expression in transgenic mouse models of Huntington's disease. Philos Trans R Soc Lond B Biol Sci. 1999;354(1386):981-989.
83. Antonini A, et al. Striatal glucose metabolism and dopamine D2 receptor binding in asymptomatic gene carriers and patients with Huntington's disease. Brain. 1996;119(pt 6):2085-2095.
84. Antonini A, Leenders KL, Eidelberg D. [11C]raclopride-PET studies of the Huntington's disease rate of progression: relevance of the trinucleotide repeat length. Ann Neurol. 1998;43(2):253-255.
85. van Oostrom JC, et al. Striatal dopamine D2 receptors, metabolism, and volume in preclinical Huntington disease. Neurology. 2005;65(6):941-943.
86. Rosas HD, et al. Striatal volume loss in HD as measured by MRI and the influence of CAG repeat. Neurology. 2001;57(6):1025-1028.
87. Aylward EH. Change in MRI striatal volumes as a biomarker in preclinical Huntington's disease. Brain Res Bull. 2007;72(2-3):152-158.
88. Feigin A, et al. Thalamic metabolism and symptom onset in preclinical Huntington's disease. Brain. 2007;130(pt 11):2858-2867.
89. Eidelberg D. Metabolic brain networks in neurodegenerative disorders: a functional imaging approach. Trends Neurosci. 2009;32(10):548-557.
90. Spetsieris PG, Eidelberg D. Scaled subprofile modeling of resting state imaging data in Parkinson's disease: methodological issues [published online ahead of print October 20, 2010]. NeuroImage. doi:10.1016/j.neuroimage.2010.10. 025.
91. Tang CC, Poston KL, Dhawan V, Eidelberg D. Abnormalities in metabolic network activity precede the onset of motor symptoms in Parkinson's disease. J Neurosci. 2010;30(3):1049-1056.
92. Langbehn DR, Brinkman RR, Falush D, Paulsen JS, Hayden MR. A new model for prediction of the age of onset and penetrance for Huntington's disease based on CAG length. Clin Genet. 2004;65(4):267-277.
93. Rosas HD, et al. Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology. 2002;58(5):695-701.
94. Rosas HD, Feigin AS, Hersch SM. Using advances in neuroimaging to detect, understand, and monitor disease progression in Huntington's disease. NeuroRx. 2004;1(2):263-272.
95. Paulsen JS, et al. Brain structure in preclinical Huntington's disease. Biol Psychiatry. 2006;59(1):57-63.
96. Tang C, et al. A metabolic network associated with the progression of preclinical Huntington's disease: application of the ordinal trends analysis to a longitudinal PET study. Neurotherapeutics. 2009;6(1):207-208.
97. Feigin A, et al. Preclinical Huntington's disease: compensatory brain responses during learning. Ann Neurol. 2006;59(1):53-59.
98. Smith Y, Raju DV, Pare JF, Sidibe M. The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci. 2004;27(9):520-527.
99. Sotrel A, Paskevich PA, Kiely DK, Bird ED, Williams RS, Myers RH. Morphometric analysis of the prefrontal cortex in Huntington's disease. Neurology. 1991;41(7):1117-1123.
100. Heinsen H, et al. Nerve cell loss in the thalamic centromedian- parafascicular complex in patients with Huntington's disease. Acta Neuropathol. 1996;91(2):161-168.
101. Heinsen H, et al. Nerve cell loss in the thalamic mediodorsal nucleus in Huntington's disease. Acta Neuropathol. 1999;97(6):613-622.
102. Kassubek J, Juengling FD, Ecker D, Landwehrmeyer GB. Thalamic atrophy in Huntington's disease covaries with cognitive performance: a morphometric MRI analysis. Cereb Cortex. 2005;15(6):846-853.
103. Mayberg HS, Starkstein SE, Peyser CE, Brandt J, Dannals RF, Folstein SE. Paralimbic frontal lobe hypometabolism in depression associated with Huntington's disease. Neurology. 1992;42(9):1791-1797.
104. Reading SA, et al. Functional brain changes in presymptomatic Huntington's disease. Ann Neurol. 2004;55(6):879-883.
105. Pavese N, et al. Microglial activation correlates with severity in Huntington disease: a clinical and PET study. Neurology. 2006;66(11):1638-1643.
106. Lodi R, et al. Abnormal in vivo skeletal muscle energy metabolism in Huntington's disease and dentatorubropallidoluysian atrophy. Ann Neurol. 2000;48(1):72-76.
107. Saft C, et al. Mitochondrial impairment in patients and asymptomatic mutation carriers of Huntington's disease. Mov Disord. 2005;20(6):674-679.
108. Koroshetz WJ, Jenkins BG, Rosen BR, Beal MF. Energy metabolism defects in Huntington's disease and effects of coenzyme Q10. Ann Neurol. 1997;41(2):160-165.
109. Gu M, Gash MT, Mann VM, Javoy-Agid F, Cooper JM, Schapira AH. Mitochondrial defect in Huntington's disease caudate nucleus. Ann Neurol. 1996;39(3):385-389.
110. Browne SE, et al. Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann Neurol. 1997;41(5):646-653.
111. Tabrizi SJ, Cleeter MW, Xuereb J, Taanman JW, Cooper JM, Schapira AH. Biochemical abnormalities and excitotoxicity in Huntington's disease brain. Ann Neurol. 1999;45(1):25-32.
112. Brouillet E, Jacquard C, Bizat N, Blum D. 3-Nitropropionic acid: a mitochondrial toxin to uncover physiopathological mechanisms underlying striatal degeneration in Huntington's disease. J Neurochem. 2005;95(6):1521-1540.
113. 15O- and FDG-PET. Int J Biomed Imag. 2006;2006:1-13.
114. Singer JD, Willett JB. Applied Longitudinal Data Analysis: Modeling Change And Event Occurrence. New York, New York, USA: Oxford University Press; 2003.
115. Feigin A, et al. Metabolic network abnormalities in early Huntington's disease: an [(18)F]FDG PET study. J Nucl Med. 2001;42(11):1591-1595.