Transmission of delta band (0.5-4 Hz) oscillations from the globus pallidus to the substantia nigra pars reticulata in dopamine depletion.
Basal ganglia
Conductance-based model
Parkinson’s disease
Synaptic inhibition
Journal
Journal of computational neuroscience
ISSN: 1573-6873
Titre abrégé: J Comput Neurosci
Pays: United States
ID NLM: 9439510
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
received:
20
01
2023
accepted:
28
04
2023
revised:
20
01
2023
medline:
8
8
2023
pubmed:
2
6
2023
entrez:
2
6
2023
Statut:
ppublish
Résumé
Parkinson's disease (PD) and animal models of PD feature enhanced oscillations in several frequency bands in the basal ganglia (BG). Past research has emphasized the enhancement of 13-30 Hz beta oscillations. Recently, however, oscillations in the delta band (0.5-4 Hz) have been identified as a robust predictor of dopamine loss and motor dysfunction in several BG regions in mouse models of PD. In particular, delta oscillations in the substantia nigra pars reticulata (SNr) were shown to lead oscillations in motor cortex (M1) and persist under M1 lesion, but it is not clear where these oscillations are initially generated. In this paper, we use a computational model to study how delta oscillations may arise in the SNr due to projections from the globus pallidus externa (GPe). We propose a network architecture that incorporates inhibition in SNr from oscillating GPe neurons and other SNr neurons. In our simulations, this configuration yields firing patterns in model SNr neurons that match those measured in vivo. In particular, we see the spontaneous emergence of near-antiphase active-predicting and inactive-predicting neural populations in the SNr, which persist under the inclusion of STN inputs based on experimental recordings. These results demonstrate how delta oscillations can propagate through BG nuclei despite imperfect oscillatory synchrony in the source site, narrowing down potential targets for the source of delta oscillations in PD models and giving new insight into the dynamics of SNr oscillations.
Identifiants
pubmed: 37266768
doi: 10.1007/s10827-023-00853-z
pii: 10.1007/s10827-023-00853-z
pmc: PMC10527635
mid: NIHMS1908672
doi:
Substances chimiques
Dopamine
VTD58H1Z2X
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
361-380Subventions
Organisme : NINDS NIH HHS
ID : R01 NS101016
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS104835
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA053014
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS125814
Pays : United States
Organisme : NINDS NIH HHS
ID : F31 NS101821
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Abbott, L. F., Varela, J., Sen, K., & Nelson, S. (1997). Synaptic depression and cortical gain control. Science, 275(5297), 221–224.
Abdi, A., Mallet, N., Mohamed, F. Y., Sharott, A., Dodson, P. D., Nakamura, K. C., Suri, S., Avery, S. V., Larvin, J. T., Garas, F. N., et al. (2015). Prototypic and arkypallidal neurons in the dopamine-intact external globus pallidus. Journal of Neuroscience, 35(17), 6667–6688.
pubmed: 25926446
Aristieta, A., Ruiz-Ortega, J., Miguelez, C., Morera-Herreras, T., & Ugedo, L. (2016). Chronic l-dopa administration increases the firing rate but does not reverse enhanced slow frequency oscillatory activity and synchronization in substantia nigra pars reticulata neurons from 6-hydroxydopamine-lesioned rats. Neurobiology of Disease, 89, 88–100.
pubmed: 26852950
Boraud, T., Brown, P., Goldberg, J. A., Graybiel, A. M., Magill, P. J. (2005). Oscillations in the basal ganglia: the good, the bad, and the unexpected. In: The basal ganglia VIII, Springer, pp 1–24
Brown, P., Oliviero, A., Mazzone, P., Insola, A., Tonali, P., & Di Lazzaro, V. (2001). Dopamine dependency of oscillations between subthalamic nucleus and pallidum in parkinson’s disease. Journal of Neuroscience, 21(3), 1033–1038.
pubmed: 11157088
Cancedda, L., & Poo, M. M. (2009). Synapse formation and elimination: competition and the role of activity. In: Binder M, Hirokawa N, Windhorst U (eds) Encyclopedia of Neuroscience, Springer, Berlin, Heidelberg, pp 3932–3938
Cassidy, M., Mazzone, P., Oliviero, A., Insola, A., Tonali, P., Lazzaro, V. D., & Brown, P. (2002). Movement-related changes in synchronization in the human basal ganglia. Brain, 125(6), 1235–1246.
pubmed: 12023312
Connelly, W. M., Schulz, J. M., Lees, G., & Reynolds, J. N. (2010). Differential short-term plasticity at convergent inhibitory synapses to the substantia nigra pars reticulata. Journal of Neuroscience, 30(44), 14854–14861.
pubmed: 21048144
Corbit, V. L., Whalen, T. C., Zitelli, K. T., Crilly, S. Y., Rubin, J. E., & Gittis, A. H. (2016). Pallidostriatal projections promote [Formula: see text] oscillations in a dopamine-depleted biophysical network model. Journal of Neuroscience, 36(20), 5556–5571.
pubmed: 27194335
DeLong, M., & Wichmann, T. (2010). Changing views of basal ganglia circuits and circuit disorders. Clinical EEG and neuroscience, 41(2), 61–67.
pubmed: 20521487
pmcid: 4305332
Du, G., Zhuang, P., Hallett, M., Zhang, Y. Q., Li, J. Y., & Li, Y. J. (2018). Properties of oscillatory neuronal activity in the basal ganglia and thalamus in patients with parkinson’s disease. Translational neurodegeneration, 7(1), 1–13.
Fino, E., Glowinski, J., & Venance, L. (2005). Bidirectional activity-dependent plasticity at corticostriatal synapses. Journal of Neuroscience, 25(49), 11279–11287.
pubmed: 16339023
Foster, N. N., Korobkova, L., Garcia, L., Gao, L., Becerra, M., Sherafat, Y., Peng, B., Li, X., Choi, J. H., Gou, L., et al. (2020). The mouse cortico-basal ganglia-thalamic network. bioRxiv
Freeze, B. S., Kravitz, A. V., Hammack, N., Berke, J. D., & Kreitzer, A. C. (2013). Control of basal ganglia output by direct and indirect pathway projection neurons. Journal of Neuroscience, 33(47), 18531–18539.
pubmed: 24259575
Gerstner, W., Kistler, W. M., Naud, R., Paninski, L. (2014). Neuronal dynamics: From single neurons to networks and models of cognition. Cambridge University Press
Halje, P., Brys, I., Mariman, J. J., da Cunha, C., Fuentes, R., & Petersson, P. (2019). Oscillations in cortico-basal ganglia circuits: Implications for parkinson’s disease and other neurologic and psychiatric conditions. Journal of Neurophysiology, 122(1), 203–231.
pubmed: 31042442
Hammond, C., Bergman, H., & Brown, P. (2007). Pathological synchronization in parkinson’s disease: networks, models and treatments. Trends in Neurosciences, 30(7), 357–364.
pubmed: 17532060
Heimer, G., Rivlin, M., Israel, Z., Bergman, H. (2006). Synchronizing activity of basal ganglia and pathophysiology of parkinson’s disease. Parkinson’s Disease and Related Disorders, pp 17–20
Higgs, M. H., & Wilson, C. J. (2016). Unitary synaptic connections among substantia nigra pars reticulata neurons. Journal of Neurophysiology, 115(6), 2814–2829.
pubmed: 26961101
pmcid: 4946591
Holt, G. R., Softky, W. R., Koch, C., & Douglas, R. J. (1996). Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. Journal of Neurophysiology, 75(5), 1806–1814.
pubmed: 8734581
Hurtado, J. M., Gray, C. M., Tamas, L. B., & Sigvardt, K. A. (1999). Dynamics of tremor-related oscillations in the human globus pallidus: a single case study. Proceedings of the National Academy of Sciences, 96(4), 1674–1679.
Hurtado, J. M., Rubchinsky, L. L., Sigvardt, K. A., Wheelock, V. L., & Pappas, C. T. (2005). Temporal evolution of oscillations and synchrony in gpi/muscle pairs in parkinson’s disease. Journal of Neurophysiology, 93(3), 1569–1584.
pubmed: 15496492
Jenkinson, N., & Brown, P. (2011). New insights into the relationship between dopamine, beta oscillations and motor function. Trends in Neurosciences, 34(12), 611–618.
pubmed: 22018805
Kita, H., & Kitai, S. (1987). Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the pha-l method. Journal of Comparative Neurology, 260(3), 435–452.
pubmed: 2439552
Levy, R., Ashby, P., Hutchison, W. D., Lang, A. E., Lozano, A. M., & Dostrovsky, J. O. (2002). Dependence of subthalamic nucleus oscillations on movement and dopamine in parkinson’s disease. Brain, 125(6), 1196–1209.
pubmed: 12023310
Lo, Y. J., & Poo, M. M. (1991). Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. Science, 254(5034), 1019–1022.
pubmed: 1658939
Mallet, N., Pogosyan, A., Márton, L. F., Bolam, J. P., Brown, P., & Magill, P. J. (2008). Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. Journal of Neuroscience, 28(52), 14245–14258.
pubmed: 19109506
Mallet, N., Micklem, B. R., Henny, P., Brown, M. T., Williams, C., Bolam, J. P., Nakamura, K. C., & Magill, P. J. (2012). Dichotomous organization of the external globus pallidus. Neuron, 74(6), 1075–1086.
pubmed: 22726837
pmcid: 3407962
McCairn, K. W., & Turner, R. S. (2009). Deep brain stimulation of the globus pallidus internus in the parkinsonian primate: local entrainment and suppression of low-frequency oscillations. Journal of Neurophysiology, 101(4), 1941–1960.
pubmed: 19164104
pmcid: 3350155
Nakano, K. (2000). Neural circuits and topographic organization of the basal ganglia and related regions. Brain and Development, 22, 5–16.
Parr-Brownlie, L. C., Poloskey, S. L., Bergstrom, D. A., & Walters, J. R. (2009). Parafascicular thalamic nucleus activity in a rat model of parkinson’s disease. Experimental Neurology, 217(2), 269–281.
pubmed: 19268664
pmcid: 2727617
Phillips, R. S., Rosner, I., Gittis, A. H., & Rubin, J. E. (2020). The effects of chloride dynamics on substantia nigra pars reticulata responses to pallidal and striatal inputs. Elife, 9, e55592.
pubmed: 32894224
pmcid: 7476764
Raz, A., Vaadia, E., & Bergman, H. (2000). Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine vervet model of parkinsonism. Journal of Neuroscience, 20(22), 8559–8571.
pubmed: 11069964
Rubin, J. E. (2017). Computational models of basal ganglia dysfunction: the dynamics is in the details. Current Opinion in Neurobiology, 46, 127–135.
pubmed: 28888856
Simmons, D. V., Higgs, M. H., Lebby, S., & Wilson, C. J. (2020). Indirect pathway control of firing rate and pattern in the substantia nigra pars reticulata. Journal of Neurophysiology, 123(2), 800–814.
pubmed: 31940230
pmcid: 7052642
Smith, Y., & Bolam, J. P. (1989). Neurons of the substantia nigra reticulata receive a dense gaba-containing input from the globus pallidus in the rat. Brain Research, 493(1), 160–167.
pubmed: 2476197
Steigerwald, F., Potter, M., Herzog, J., Pinsker, M., Kopper, F., Mehdorn, H., Deuschl, G., & Volkmann, J. (2008). Neuronal activity of the human subthalamic nucleus in the parkinsonian and nonparkinsonian state. Journal of Neurophysiology, 100(5), 2515–2524.
pubmed: 18701754
Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science, 262(5134), 679–685.
pubmed: 8235588
Terman, D., Rubin, J. E., Yew, A., & Wilson, C. (2002). Activity patterns in a model for the subthalamopallidal network of the basal ganglia. Journal of Neuroscience, 22(7), 2963–2976.
pubmed: 11923461
Thoenen, H. (2000). Neurotrophins and activity-dependent plasticity. Progress in Brain Research, 128, 183–191.
pubmed: 11105678
Tseng, K. Y., Kasanetz, F., Kargieman, L., Riquelme, L. A., & Murer, M. G. (2001). Cortical slow oscillatory activity is reflected in the membrane potential and spike trains of striatal neurons in rats with chronic nigrostriatal lesions. Journal of Neuroscience, 21(16), 6430–6439.
pubmed: 11487667
Turrigiano, G. G. (2008). The self-tuning neuron: synaptic scaling of excitatory synapses. Cell, 135(3), 422–435.
pubmed: 18984155
pmcid: 2834419
Walters, J. R., Hu, D., Itoga, C. A., Parr-Brownlie, L. C., & Bergstrom, D. A. (2007). Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine. Neuroscience, 144(2), 762–776.
pubmed: 17112675
Weinberger, M., Mahant, N., Hutchison, W. D., Lozano, A. M., Moro, E., Hodaie, M., Lang, A. E., & Dostrovsky, J. O. (2006). Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in parkinson’s disease. Journal of Neurophysiology, 96(6), 3248–3256.
pubmed: 17005611
Whalen, T. C., Willard, A. M., Rubin, J. E., & Gittis, A. H. (2020). Delta oscillations are a robust biomarker of dopamine depletion severity and motor dysfunction in awake mice. Journal of Neurophysiology, 124(2), 312–329.
pubmed: 32579421
pmcid: 7500379
Willard, A. M., Isett, B. R., Whalen, T. C., Mastro, K. J., Ki, C. S., Mao, X., & Gittis, A. H. (2019). State transitions in the substantia nigra reticulata predict the onset of motor deficits in models of progressive dopamine depletion in mice. Elife, 8, e42746.
pubmed: 30839276
pmcid: 6402832
Xia, X. M., Fakler, B., Rivard, A., Wayman, G., Johnson-Pais, T., Keen, J., Ishii, T., Hirschberg, B., Bond, C., Lutsenko, S., et al. (1998). Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature, 395(6701), 503.
pubmed: 9774106
Yelnik, A. P., Lebreton, F. O., Bonan, I. V., Colle, F. M., Meurin, F. A., Guichard, J. P., & Vicaut, E. (2002). Perception of verticality after recent cerebral hemispheric stroke. Stroke, 33(9), 2247–2253.
pubmed: 12215595
Zhou, F. W., Matta, S. G., & Zhou, F. M. (2008). Constitutively active trpc3 channels regulate basal ganglia output neurons. Journal of Neuroscience, 28(2), 473–482.
pubmed: 18184790
Zhou, F. W., Jin, Y., Matta, S. G., Xu, M., & Zhou, F. M. (2009). An ultra-short dopamine pathway regulates basal ganglia output. Journal of Neuroscience, 29(33), 10424–10435.
pubmed: 19692618
Zhuang, P., Hallett, M., Meng, D., Zhang, Y., & Li, Y. (2019). Characteristics of oscillatory activity in the globus pallidus internus in patients with parkinson’s disease (p1.8-028). Neurology, 92(15 Supplement).