DOI: 10.1523/jneurosci.5687-08.2009. Age-Dependent Alterations of Corticostriatal Activity in the YAC128 Mouse Model of Huntington Disease

Age-Dependent Alterations of Corticostriatal Activity in the YAC128 Mouse Model of Huntington Disease

10.1523/jneurosci.5687-08.2009

Crossref journal-article

Society for Neuroscience

The Journal of Neuroscience (393)

Abstract

Huntington disease is a genetic neurodegenerative disorder that produces motor, neuropsychiatric, and cognitive deficits and is caused by an abnormal expansion of the CAG tract in the huntingtin (htt) gene. In humans, mutated htt induces a preferential loss of medium spiny neurons in the striatum and, to a lesser extent, a loss of cortical neurons as the disease progresses. The mechanisms causing these degenerative changes remain unclear, but they may involve synaptic dysregulation. We examined the activity of the corticostriatal pathway using a combination of electrophysiological and optical imaging approaches in brain slices and acutely dissociated neurons from the YAC128 mouse model of Huntington disease. The results demonstrated biphasic age-dependent changes in corticostriatal function. At 1 month, before the behavioral phenotype develops, synaptic currents and glutamate release were increased. At 7 and 12 months, after the development of the behavioral phenotype, evoked synaptic currents were reduced. Glutamate release was decreased by 7 months and was markedly reduced by 12 months. These age-dependent alterations in corticostriatal activity were paralleled by a decrease in dopamine D2receptor modulation of the presynaptic terminal. Together, these findings point to dynamic alterations at the corticostriatal pathway and emphasize that therapies directed toward preventing or alleviating symptoms need to be specifically designed depending on the stage of disease progression.

Bibliography

Joshi, P. R., Wu, N.-P., AndrÃ©, V. M., Cummings, D. M., Cepeda, C., Joyce, J. A., Carroll, J. B., Leavitt, B. R., Hayden, M. R., Levine, M. S., & Bamford, N. S. (2009). Age-Dependent Alterations of Corticostriatal Activity in the YAC128 Mouse Model of Huntington Disease. The Journal of Neuroscience, 29(8), 2414â2427.

Authors 11

Prasad R. Joshi (first)
Nan-Ping Wu (additional)
Véronique M. André (additional)
Damian M. Cummings (additional)
Carlos Cepeda (additional)
John A. Joyce (additional)
Jeffrey B. Carroll (additional)
Blair R. Leavitt (additional)
Michael R. Hayden (additional)
Michael S. Levine (additional)
Nigel S. Bamford (additional)

References 67 Referenced 142

10.1016/0166-2236(89)90074-X
10.1002/ana.410270403
10.1152/jn.01118.2005
10.1002/jnr.10272
10.1152/jn.00791.2004
10.1523/JNEUROSCI.2891-04.2004
10.1016/S0896-6273(04)00265-X
10.1016/j.neuron.2008.01.033
10.1523/JNEUROSCI.14-11-06667.1994 / J Neurosci / Cellular and molecular characterization of Ca2+ currents in acutely isolated, adult rat neostriatal neurons by Bargas (1994)
10.1016/j.neuroscience.2007.03.010
10.1126/science.1553547
10.1111/j.1460-9568.1995.tb00689.x
10.1152/jn.1998.79.1.82 / J Neurophysiol / Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons in slices: contribution of calcium conductances by Cepeda (1998)
10.1002/jnr.1244
10.1523/JNEUROSCI.23-03-00961.2003 / J Neurosci / Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease by Cepeda (2003)
10.1016/j.pneurobio.2006.11.001
10.1111/j.1460-9568.2008.06038.x
10.1016/j.neuron.2004.05.008
10.1016/0166-2236(90)90111-M
10.1016/S0006-8993(98)01095-6
10.1016/S0022-3565(24)38033-4 / J Pharmacol Exp Ther / Age-related changes in the capacity, rate, and modulation of dopamine uptake within the striatum and nucleus accumbens of Fischer 344 rats: an in vivo electrochemical study by Hebert (1999)
10.1523/JNEUROSCI.1830-07.2007
10.1016/0092-8674(93)90585-E
10.1016/S0896-6273(01)80053-2
10.1111/j.1471-4159.2006.03762.x
10.1111/j.1471-4159.2007.04908.x
10.1016/S0896-6273(00)81029-6
10.1152/jn.2001.86.6.2667 / J Neurophysiol / Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice by Klapstein (2001)
10.1038/nature05506
10.1523/JNEUROSCI.21-23-09112.2001 / J Neurosci / Changes in cortical and striatal neurons predict behavioral and electrophysiological abnormalities in a transgenic murine model of Huntington's disease by Laforet (2001)
10.1523/JNEUROSCI.1990-04.2004
10.1096/fj.08-107268
10.1002/(SICI)1097-4547(19991115)58:4<515::AID-JNR5>3.0.CO;2-F
10.1093/hmg/ddg218
10.1016/j.molmed.2003.08.006
10.1152/jn.00308.2004
10.1056/NEJM199403033300907
10.1038/382363a0
10.1006/meth.1999.0776
10.1016/S0092-8674(00)81369-0
10.1016/0165-0173(90)90011-C
10.1113/jphysiol.2007.142448
10.1177/1073858407305833
10.1016/S0026-895X(25)08654-7 / Mol Pharmacol / Cyclothiazide differentially modulates desensitization of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor splice variants by Partin (1994)
10.1016/0896-6273(95)90227-9
10.1073/pnas.85.15.5733
10.1002/ana.410370309
10.1097/00001756-200108080-00051
10.1016/0896-6273(93)90081-2
10.1016/0306-4522(94)00427-7
10.1097/00005072-199902000-00006
10.1523/JNEUROSCI.21-16-05916.2001 / J Neurosci / Amphetamine distorts stimulation-dependent dopamine overflow: effects on D2 autoreceptors, transporters, and synaptic vesicle stores by Schmitz (2001)
10.1016/j.nbd.2005.08.001
10.1093/hmg/ddg169
10.1007/s00018-005-5084-5
10.1002/jnr.20651
10.1152/jn.1997.77.4.1697 / J Neurophysiol / Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo by Stern (1997)
10.1073/pnas.92.3.846
10.1002/syn.1089
10.1038/2807
10.1073/pnas.110078997
10.1523/JNEUROSCI.0590-05.2005
10.1097/00005072-199805000-00001
10.1046/j.1460-9568.2000.00175.x
10.1523/JNEUROSCI.23-18-07059.2003 / J Neurosci / Presynaptic capacitance measurements and Ca2+ uncaging reveal submillisecond exocytosis kinetics and characterize the Ca2+ sensitivity of vesicle pool depletion at a fast CNS synapse by Wölfel (2003)
10.1172/JCI200317742
10.1038/89498

Dates

Type	When
Created	16 years, 6 months ago (Feb. 25, 2009, 1:34 p.m.)
Deposited	6 months, 3 weeks ago (Feb. 7, 2025, 5:22 p.m.)
Indexed	4 days, 19 hours ago (Aug. 26, 2025, 2:47 a.m.)
Issued	16 years, 6 months ago (Feb. 25, 2009)
Published	16 years, 6 months ago (Feb. 25, 2009)
Published Online	16 years, 6 months ago (Feb. 25, 2009)
Published Print	16 years, 6 months ago (Feb. 25, 2009)

Funders 0

None

BibTeX

@article{Joshi_2009, title={Age-Dependent Alterations of Corticostriatal Activity in the YAC128 Mouse Model of Huntington Disease}, volume={29}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.5687-08.2009}, DOI={10.1523/jneurosci.5687-08.2009}, number={8}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Joshi, Prasad R. and Wu, Nan-Ping and André, Véronique M. and Cummings, Damian M. and Cepeda, Carlos and Joyce, John A. and Carroll, Jeffrey B. and Leavitt, Blair R. and Hayden, Michael R. and Levine, Michael S. and Bamford, Nigel S.}, year={2009}, month=feb, pages={2414–2427} }

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