Neuroanatomical Visualization of the Impaired Striatal Connectivity in Huntington's Disease Mouse Model
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  • 作者:Dohee Kim ; Jeha Jeon ; Eunji Cheong ; Dong Jin Kim ; Hoon Ryu…
  • 关键词:Striatum ; Huntington’s disease ; YAC128 ; Basal ganglia ; Amygdala ; Neurotracer
  • 刊名:Molecular Neurobiology
  • 出版年:2016
  • 出版时间:May 2016
  • 年:2016
  • 卷:53
  • 期:4
  • 页码:2276-2286
  • 全文大小:1,000 KB
  • 参考文献:1.Group THsDCR (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cell 72(6):971–983CrossRef
    2.Vonsattel JP, DiFiglia M (1998) Huntington disease. J Neuropathol Exp Neurol 57(5):369–384CrossRef PubMed
    3.Caine ED, Shoulson I (1983) Psychiatric syndromes in Huntington’s disease. Am J Psychiatry 140(6):728–733CrossRef PubMed
    4.Julien CL, Thompson JC, Wild S, Yardumian P, Snowden JS, Turner G, Craufurd D (2007) Psychiatric disorders in preclinical Huntington’s disease. J Neurol Neurosurg Psychiatry 78(9):939–943CrossRef PubMed PubMedCentral
    5.Paulsen JS (2011) Cognitive impairment in Huntington disease: diagnosis and treatment. Curr Neurol Neurosci Rep 11(5):474–483. doi:10.​1007/​s11910-011-0215-x CrossRef PubMed PubMedCentral
    6.Snowden JS, Craufurd D, Griffiths HL, Neary D (1998) Awareness of involuntary movements in Huntington disease. Arch Neurol 55(6):801–805CrossRef PubMed
    7.Cummings DM, Cepeda C, Levine MS (2010) Alterations in striatal synaptic transmission are consistent across genetic mouse models of Huntington’s disease. ASN Neuro 2(3):e00036. doi:10.​1042/​AN20100007 CrossRef PubMed PubMedCentral
    8.Clark VP, Lai S, Deckel AW (2002) Altered functional MRI responses in Huntington’s disease. Neuroreport 13(5):703–706CrossRef PubMed
    9.Andre VM, Cepeda C, Fisher YE, Huynh M, Bardakjian N, Singh S, Yang XW, Levine MS (2011) Differential electrophysiological changes in striatal output neurons in Huntington’s disease. J Neurosci 31(4):1170–1182. doi:10.​1523/​JNEUROSCI.​3539-10.​2011 CrossRef PubMed PubMedCentral
    10.Klapstein GJ, Fisher RS, Zanjani H, Cepeda C, Jokel ES, Chesselet MF, Levine MS (2001) Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington’s disease transgenic mice. J Neurophysiol 86(6):2667–2677PubMed
    11.Kloppel S, Henley SM, Hobbs NZ, Wolf RC, Kassubek J, Tabrizi SJ, Frackowiak RS (2009) Magnetic resonance imaging of Huntington’s disease: preparing for clinical trials. Neuroscience 164(1):205–219. doi:10.​1016/​j.​neuroscience.​2009.​01.​045 CrossRef PubMed PubMedCentral
    12.Cepeda-Prado E, Popp S, Khan U, Stefanov D, Rodriguez J, Menalled LB, Dow-Edwards D, Small SA et al (2012) R6/2 Huntington’s disease mice develop early and progressive abnormal brain metabolism and seizures. J Neurosci 32(19):6456–6467. doi:10.​1523/​JNEUROSCI.​0388-12.​2012 CrossRef PubMed PubMedCentral
    13.Slow EJ, van Raamsdonk J, Rogers D, Coleman SH, Graham RK, Deng Y, Oh R, Bissada N et al (2003) Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum Mol Genet 12(13):1555–1567CrossRef PubMed
    14.Van Raamsdonk JM, Pearson J, Slow EJ, Hossain SM, Leavitt BR, Hayden MR (2005) Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington’s disease. J Neurosci 25(16):4169–4180. doi:10.​1523/​JNEUROSCI.​0590-05.​2005 CrossRef PubMed
    15.Van Raamsdonk JM, Murphy Z, Slow EJ, Leavitt BR, Hayden MR (2005) Selective degeneration and nuclear localization of mutant huntingtin in the YAC128 mouse model of Huntington disease. Hum Mol Genet 14(24):3823–3835. doi:10.​1093/​hmg/​ddi407 CrossRef PubMed
    16.Tepper JM, Abercrombie ED, Bolam JP (2007) Basal ganglia macrocircuits. Prog Brain Res 160:3–7. doi:10.​1016/​S0079-6123(06)60001-0 CrossRef PubMed
    17.Joshi PR, Wu NP, Andre VM, Cummings DM, Cepeda C, Joyce JA, Carroll JB, Leavitt BR et al (2009) Age-dependent alterations of corticostriatal activity in the YAC128 mouse model of Huntington disease. J Neurosci 29(8):2414–2427. doi:10.​1523/​JNEUROSCI.​5687-08.​2009 CrossRef PubMed PubMedCentral
    18.Tang T-S, Chen X, Liu J, Bezprozvanny I (2007) Dopaminergic signaling and striatal neurodegeneration in Huntington’s disease. J Neurosci 27(30):7899–7910CrossRef PubMed PubMedCentral
    19.Franklin KB, Paxinos G (1997) Mouse brain in stereotaxic coordinates. Academic Press, San Diego
    20.Van Raamsdonk JM, Pearson J, Rogers DA, Bissada N, Vogl AW, Hayden MR, Leavitt BR (2005) Loss of wild-type huntingtin influences motor dysfunction and survival in the YAC128 mouse model of Huntington disease. Hum Mol Genet 14(10):1379–1392. doi:10.​1093/​hmg/​ddi147 CrossRef PubMed
    21.Noh H, Jeon J, Seo H (2014) Systemic injection of LPS induces region-specific neuroinflammation and mitochondrial dysfunction in normal mouse brain. Neurochem Int 69:35–40. doi:10.​1016/​j.​neuint.​2014.​02.​008 CrossRef PubMed
    22.Honig MG, Hume RI (1989) Dil and diO: versatile fluorescent dyes for neuronal labelling and pathway tracing. Trends Neurosci 12(9):333–341CrossRef PubMed
    23.Fonnum F, Storm-Mathisen J, Divac I (1981) Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in rat brain. Neuroscience 6(5):863–873CrossRef PubMed
    24.Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13(4):400–408CrossRef PubMed
    25.Pan WX, Mao T, Dudman JT (2010) Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. Front Neuroanat 4:147. doi:10.​3389/​fnana.​2010.​00147 CrossRef PubMed PubMedCentral
    26.Wall NR, De La Parra M, Callaway EM, Kreitzer AC (2013) Differential innervation of direct- and indirect-pathway striatal projection neurons. Neuron 79(2):347–360. doi:10.​1016/​j.​neuron.​2013.​05.​014 CrossRef PubMed PubMedCentral
    27.Gomez-Tortosa E, del Barrio A, Barroso T, Garcia Ruiz PJ (1996) Visual processing disorders in patients with Huntington’s disease and asymptomatic carriers. J Neurol 243(3):286–292CrossRef PubMed
    28.Smith Y, Raju D, Nanda B, Pare JF, Galvan A, Wichmann T (2009) The thalamostriatal systems: anatomical and functional organization in normal and parkinsonian states. Brain Res Bull 78(2–3):60–68. doi:10.​1016/​j.​brainresbull.​2008.​08.​015 CrossRef PubMed PubMedCentral
    29.Kimura M (1992) Behavioral modulation of sensory responses of primate putamen neurons. Brain Res 578(1):204–214CrossRef PubMed
    30.Minamimoto T, Hori Y, Kimura M (2005) Complementary process to response bias in the centromedian nucleus of the thalamus. Science 308(5729):1798–1801. doi:10.​1126/​science.​1109154 CrossRef PubMed
    31.Minamimoto T, Kimura M (2002) Participation of the thalamic CM–Pf complex in attentional orienting. J Neurophysiol 87(6):3090–3101. doi:10.​1152/​jn.​00564.​2001 PubMed
    32.Heinsen H, Rub U, Gangnus D, Jungkunz G, Bauer M, Ulmar G, Bethke B, Schuler M et al (1996) Nerve cell loss in the thalamic centromedian–parafascicular complex in patients with Huntington’s disease. Acta Neuropathol 91(2):161–168CrossRef PubMed
    33.Henderson JM, Carpenter K, Cartwright H, Halliday GM (2000) Loss of thalamic intralaminar nuclei in progressive supranuclear palsy and Parkinson’s disease: clinical and therapeutic implications. Brain J Neurol 123(Pt 7):1410–1421CrossRef
    34.Chen JY, Wang EA, Cepeda C, Levine MS (2013) Dopamine imbalance in Huntington’s disease: a mechanism for the lack of behavioral flexibility. Front Neurosci 7:114. doi:10.​3389/​fnins.​2013.​00114 PubMed PubMedCentral
    35.Vijayraghavan S, Wang M, Birnbaum SG, Williams GV, Arnsten AF (2007) Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat Neurosci 10(3):376–384. doi:10.​1038/​nn1846 CrossRef PubMed
    36.Callahan JW, Abercrombie ED (2011) In vivo dopamine efflux is decreased in striatum of both fragment (R6/2) and full-length (YAC128) transgenic mouse models of Huntington’s disease. Front Syst Neurosci 5:61. doi:10.​3389/​fnsys.​2011.​00061 CrossRef PubMed PubMedCentral
    37.Petersen A, Puschban Z, Lotharius J, NicNiocaill B, Wiekop P, O’Connor WT, Brundin P (2002) Evidence for dysfunction of the nigrostriatal pathway in the R6/1 line of transgenic Huntington’s disease mice. Neurobiol Dis 11(1):134–146CrossRef PubMed
    38.Gray TS (1999) Functional and anatomical relationships among the amygdala, basal forebrain, ventral striatum, and cortex: an integrative discussion. Ann N Y Acad Sci 877(1):439–444CrossRef PubMed
    39.Lidov HG, Molliver ME (1982) An immunohistochemical study of serotonin neuron development in the rat: ascending pathways and terminal fields. Brain Res Bull 8(4):389–430CrossRef PubMed
    40.Hare TA, Tottenham N, Davidson MC, Glover GH, Casey BJ (2005) Contributions of amygdala and striatal activity in emotion regulation. Biol Psychiat 57(6):624–632. doi:10.​1016/​j.​biopsych.​2004.​12.​038 CrossRef PubMed
    41.Yu H, Zhou Z, Zhou X (2013) The amygdalostriatal and corticostriatal effective connectivity in anticipation and evaluation of facial attractiveness. Brain Cog 82(3):291–300. doi:10.​1016/​j.​bandc.​2013.​04.​011 CrossRef
    42.Zorrilla EP, Koob GF (2013) Amygdalostriatal projections in the neurocircuitry for motivation: a neuroanatomical thread through the career of Ann Kelley. Neurosci Biobehav Rev 37(9 Pt A):1932–1945. doi:10.​1016/​j.​neubiorev.​2012.​11.​019 CrossRef PubMed
    43.Mann DM, Oliver R, Snowden JS (1993) The topographic distribution of brain atrophy in Huntington’s disease and progressive supranuclear palsy. Acta Neuropathol 85(5):553–559CrossRef PubMed
    44.Smolinsky AN, Bergner CL, LaPorte JL, Kalueff AV (2009) Analysis of grooming behavior and its utility in studying animal stress, anxiety, and depression. In: Mood and anxiety related phenotypes in mice. Springer, pp 21–36
    45.Kalueff AV, Tuohimaa P (2005) Contrasting grooming phenotypes in three mouse strains markedly different in anxiety and activity (129S1, BALB/c and NMRI). Behav Brain Res 160(1):1–10CrossRef PubMed
    46.Kalueff AV, Tuohimaa P (2005) The grooming analysis algorithm discriminates between different levels of anxiety in rats: potential utility for neurobehavioural stress research. J Neurosci Methods 143(2):169–177CrossRef PubMed
    47.DeLong M (2000) The basal ganglia. In: Kandel ER, Schwartz JH, Jessell TM (eds) Principles of neural science. McGraw-Hill, New York, pp 853–867
    48.Kandel ER, Schwartz JH, Jessell TM (2000) Principles of neural science, vol 4. McGraw-Hill, New York
    49.Wolf RC, Sambataro F, Vasic N, Wolf ND, Thomann PA, Landwehrmeyer GB, Orth M (2011) Longitudinal functional magnetic resonance imaging of cognition in preclinical Huntington’s disease. Exp Neurol 231(2):214–222CrossRef PubMed
    50.Wolf RC, Sambataro F, Vasic N, Depping MS, Thomann PA, Landwehrmeyer GB, Sussmuth SD, Orth M (2014) Abnormal resting-state connectivity of motor and cognitive networks in early manifest Huntington’s disease. Psychol Med 44(15):3341–3356. doi:10.​1017/​S003329171400057​9 CrossRef PubMed
    51.Poudel GR, Egan GF, Churchyard A, Chua P, Stout JC, Georgiou-Karistianis N (2014) Abnormal synchrony of resting state networks in premanifest and symptomatic Huntington disease: the IMAGE-HD study. J Psychiatry Neurosci 39(2):87PubMed PubMedCentral
    52.Gray M, Egan G, Ando A, Churchyard A, Chua P, Stout J, Georgiou-Karistianis N (2013) Prefrontal activity in Huntington’s disease reflects cognitive and neuropsychiatric disturbances: the IMAGE-HD study. Exp Neurol 239:218–228CrossRef PubMed
    53.Ferraro S, Nanetti L, Piacentini S, Mandelli ML, Bertolino N, Ghielmetti F, Epifani F, Nigri A et al (2014) Frontal cortex BOLD signal changes in premanifest Huntington disease A possible fMRI biomarker. Neurology 83(1):65–72CrossRef PubMed PubMedCentral
    54.Ferris CF, Kulkarni P, Toddes S, Yee J, Kenkel W, Nedelman M (2014) Studies on the Q175 knock-in model of Huntington’s disease using functional imaging in awake mice: evidence of olfactory dysfunction. Front Neurol 5:94CrossRef PubMed PubMedCentral
    55.Stack EC, Kubilus JK, Smith K, Cormier K, Del Signore SJ, Guelin E, Ryu H, Hersch SM et al (2005) Chronology of behavioral symptoms and neuropathological sequela in R6/2 Huntington’s disease transgenic mice. J Comp Neurol 490(4):354–370CrossRef PubMed
    56.Arnulf I, Nielsen J, Lohmann E, Schiefer J, Wild E, Jennum P, Konofal E, Walker M et al (2008) Rapid eye movement sleep disturbances in Huntington disease. JAMA Neurol 65(4):482–488. doi:10.​1001/​archneur.​65.​4.​482
    57.Dogan I, Sass C, Mirzazade S, Kleiman A, Werner CJ, Pohl A, Schiefer J, Binkofski F et al (2014) Neural correlates of impaired emotion processing in manifest Huntington’s disease. Soc Cogn Affect Neur 9(5):671–680. doi:10.​1093/​scan/​nst029 CrossRef
    58.Ille R, Holl AK, Kapfhammer HP, Reisinger K, Schafer A, Schienle A (2011) Emotion recognition and experience in Huntington’s disease: is there a differential impairment? Psychiatry Res 188(3):377–382. doi:10.​1016/​j.​psychres.​2011.​04.​007 CrossRef PubMed PubMedCentral
    59.Sprengelmeyer R, Young AW, Calder AJ, Karnat A, Lange H, Homberg V, Perrett DI, Rowland D (1996) Loss of disgust. Perception of faces and emotions in Huntington’s disease. Brain J Neurol 119(Pt 5):1647–1665CrossRef
    60.Yoshimura N, Kawamura M, Masaoka Y, Homma I (2005) The amygdala of patients with Parkinson’s disease is silent in response to fearful facial expressions. Neuroscience 131(2):523–534. doi:10.​1016/​j.​neuroscience.​2004.​09.​054 CrossRef PubMed
  • 作者单位:Dohee Kim (1) (2)
    Jeha Jeon (3)
    Eunji Cheong (2)
    Dong Jin Kim (1)
    Hoon Ryu (1) (4)
    Hyemyung Seo (3)
    Yun Kyung Kim (1) (5)

    1. Center for Neuro-Medicine, Brain Science Institute, Korea Institute of Science and Technology (KIST), Hwarangno 14-gil 5, Seongbuk-gu, Seoul, 136-791, South Korea
    2. Department of Biotechnology, College of Life Science and Biotechnology, Yonsei University, Seoul, 120-749, South Korea
    3. Department of Molecular and Life Sciences, Hanyang University, Gyeonggi-do, 426-791, South Korea
    4. Boston University Alzheimer’s Disease Center, Boston University School of Medicine, Boston, MA, USA
    5. Biological Chemistry, University of Science and Technology (UST), Daejeon, 305-333, South Korea
  • 刊物主题:Neurosciences; Neurobiology; Cell Biology; Neurology;
  • 出版者:Springer US
  • ISSN:1559-1182
文摘
Huntington’s disease (HD) is a movement disorder characterized by the early selective degeneration of striatum. For motor control, the striatum receives excitatory inputs from multiple brain regions and projects the information to other basal ganglia nuclei. Despite the pathological importance of the striatal degeneration in HD, there are little anatomical data that show impaired striatal connectivity in HD. For the anatomical mapping of the striatum, we injected here a neurotracer DiD to the dorsal striatum of HD mouse model (YAC128). Compared with littermate controls, the number of the traced inputs to the striatum was reduced dramatically in YAC128 mice at 12 months of age suggesting massive destruction of the striatal connections. Basal ganglia inputs were significantly damaged in HD mice by showing 61 % decrease in substantia nigra pars compacta, 85 % decrease in thalamic centromedian nucleus, and 55 % decrease in thalamic parafascicular nucleus. Cortical inputs were also greatly decreased by 43 % in motor cortex, 48 % in somatosensory cortex, and 72 % in visual cortex. Besides the known striatal connections, the neurotracer DiD also traced inputs from amygdala and the amygdala inputs were decreased by 68 % in YAC128 mice. Considering the role of amygdala in emotion processing, the impairment in amygdalostriatal connectivity strongly suggests that emotional disturbances could occur in HD mice. Indeed, open-field tests further indicated that YAC128 mice exhibited changes in emotional behaviors related to symptoms of depression and anxiety. Although onset of HD is clinically determined on the basis of motor abnormality, emotional deficits are also common features of the disease. Therefore, our anatomical connectivity mapping of the striatum provides a new insight to interpret brain dysfunction in HD.

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