Cerebellar and Olfactory Bulb Perturbations Induced by Vanadium Neurotoxicity in the African Giant Rat (Cricetomys gambianus, Waterhouse)
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Keywords

cerebellum
olfaction
olfactory dysfunction
glomeruli
vanadium
neurotoxicity

How to Cite

Mustapha, O., Omojola, F., Olaolorun, F., & Olude, M. (2023). Cerebellar and Olfactory Bulb Perturbations Induced by Vanadium Neurotoxicity in the African Giant Rat (Cricetomys gambianus, Waterhouse). Nigerian Journal of Physiological Sciences, 38(2), 135–143. https://doi.org/10.54548/njps.v38i2.3

Abstract

The African giant rat, AGR (Cricetomys gambianus) is a unique rodent known for its keen sense of smell which has enabled its use in the diagnosis of tuberculosis and demining activities in war torn countries. This keen sense of smell and the ability to navigate tight spaces are skills modulated by the olfactory bulb and cerebellum. While the brain is generally susceptible to environmental pollutants such as heavy metals, vanadium has predilection for these two brain regions. This work was thus designed to investigate the probable neurotoxic effect of vanadium on the neuronal cytoarchitecture of the cerebellum and olfactory bulb in this rodent. To achieve this, twelve adults male AGRs were divided into two groups (vanadium and control groups) and were given intraperitoneal injections of 3mg/kg body weight sodium metavanadate and normal saline respectively for 14 days. After which they were sacrificed, and brains harvested for histological investigations using Nissl and Golgi staining techniques. Results from our experiment revealed Purkinje cell degeneration and pyknosis as revealed by a lower intact-pyknotic cell (I-P) ratio, higher pyknotic Purkinje cell density and poor dendritic arborizations in the molecular layer of the cerebellum in the vanadium treated group. In the olfactory bulb, neuronal loss in the glomerular layer was observed as shrunken glomeruli. These neuronal changes have been linked to deficits in motor function and disruption of odor transduction in the olfactory bulb. This work has further demonstrated the neurotoxic effects of vanadium on the cerebellum and olfactory bulb of the AGR and the likely threat it may pose to the translational potentials of this rodent. We therefore propose the use of this rodent as a suitable model for better understanding vanadium induced olfactory and cerebellar dysfunctions.

https://doi.org/10.54548/njps.v38i2.3
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References

Adekanmbi, A. J., and Olude, M. A. (2021). An alternate prospect in detecting presymptomatic and asymptomatic COVID-19 carriers through odor differentiation by HeroRATs. J. Vet. Behav. 42: 26-29. https://doi.org/10.1016/j.jveb.2020.12.001

Azeez, I. A., Olopade, F., Laperchia, C., Andrioli, A., Scambi, I., Onwuka, S. K., Bentivoglio, M., and Olopade, J. O. (2016). Regional myelin and axon damage and neuroinflammation in the adult mouse brain after long exposure. J. Neuropathol. Exp. Neurol., 75(9):843-854. https://doi.org/10.1093/jnen/nlw058.

Ebokaiwe A. P., Adedara I. A., Owoeye O. and Farombi E. O. (2013). Neurotoxicity of Nigerian bonny light crude oil in rats. Drug Chem. Toxicol. 36(2): 187-195. doi: 10.3109/01480545.2012.710619

Bandyopadhyay U., Das D., and Banerjee R. K. (1999). Reactive oxygen species: Oxidative damage and pathogenesis. Curr. Sci. 77(5): 658-666.

Beckers, A., and Moons, L. (2019). Dendritic shrinkage after injury: a cellular killer or a necessity for axonal regeneration? Neural Regen. Res. 14(8): 1313–1316. https://doi.org/10.4103/1673-5374.253505

Bostan, A. C., and Strick, P. L. (2018). The basal ganglia and the cerebellum: nodes in an integrated network. Nat. Rev. Neurosci. 19: 338–350. doi: 10.1038/s41583-018-0002-7

Bostan, A. C., Dum, R. P., and Strick, P. L. (2010). The basal ganglia communicate with the cerebellum. Proc. Natl. Acad. Sci. USA. 107(18): 8452–8456. https://doi.org/10.1073/pnas.1000496107

Briffa, J., Sinagra, E., and Blundell, R. (2020). Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6(9): e04691. https://doi.org/10.1016/j.heliyon.2020.e04691

Caicedo M., Jacobs J. J., Reddy A., and Hallab N. J. (2008). Analysis of metal ion-induced DNA damage, apoptosis, and necrosis in human (Jurkat) T-cells demonstrates Ni2+ and V3+ are more toxic than other metals: Al3+, Be2+, Co2+, Cr3+, Cu2+, Fe3+, Mo5+, Nb5+, Zr2+. J. Biomed. Mater. Res. 86: 905–913.

Calvo-Ochoa, E., and Byrd-Jacobs, C. A. (2019). The Olfactory System of Zebrafish as a Model for the Study of Neurotoxicity and Injury: Implications for Neuroplasticity and Disease. Int. J. Mol. Sci. 20(7): 1639. https://doi.org/10.3390/ijms20071639

Campbell J. (2011). ‘HeroRATs’ corner landmines and tuberculosis in Africa. https://www.cfr.org/blog/herorats-corner-landmines-and-tuberculosis-africa. Date accessed: January 6,2023

Chakraborty T., Samanta S., Ghosh B., Thirumoorthy N., and Chatterjee M. (2005). Vanadium induces apoptosis and modulates the expressions of metallothionein, Ki-67 nuclear antigen, and p53 during 2-acetylaminofluorene-induced rat liver preneoplasia. J. Cell Biochem. 94: 744–762.

Chen, L., Liu, J., Hu, W., Gao, J., and Yang, J. (2021). Vanadium in soil-plant system: Source, fate, toxicity, and bioremediation. J. Hazard. Mater. 405: 124200. https://doi.org/10.1016/j.jhazmat.2020.124200

Cheng A. (2022). Magawa, ‘hero rat’ who sniffed out 71 land mines with his tiny nose, dies in retirement. The Washington Post. https://www.washingtonpost.com/world/2022/01/12/magawa-african-landmine-rat-dies-cambodia/. Date accessed: January 6, 2023.

Choe, M., Cortés, E., Vonsattel, J. P., Kuo, S. H., Faust, P. L., and Louis, E. D. (2016). Purkinje cell loss in essential tremor: Random sampling quantification and nearest neighbor analysis. Mov. Disord. 31(3): 393–401. https://doi.org/10.1002/mds.26490

Colín-Barenque, L., Pedraza-Chaverri, J., Medina-Campos, O., Jimenez-Martínez, R., Bizarro-Nevares, P., González-Villalva, A., Rojas-Lemus, M., and Fortoul, T. I. (2015). Functional and morphological olfactory bulb modifications in mice after vanadium inhalation. Toxicol. Pathol. 43(2): 282–291. https://doi.org/10.1177/0192623314548668

Cooper, R.G. (2008). Care, husbandry and diseases of the African giant rat (Cricetomys gambianus): Review Article. J. S. Afr. Vet. Assoc. 79(2): 62-66. https://doi.org/10.4102/jsava.v79i2.245

Czarnecki L. A., Moberly A. H., Turkel D. J., Rubinstein T., Pottackal J., Rosenthal M. C., McCandlish E. M. K, Buckley B., and McGann J. P. (2012). Functional Rehabilitation of Cadmium-Induced Neurotoxicity Despite Persistent Peripheral Pathophysiology in the Olfactory System, Toxicol. Sci. 126(2): 534–544. https://doi.org/10.1093/toxsci/kfs030

Davila, N. G., Blakemore, L. J., and Trombley, P. Q. (2003). Dopamine modulates synaptic transmission between rat olfactory bulb neurons in culture. J. Neurophysiol. 90(1): 395-404.

Duchamp-Viret, P., Coronas, V., Delaleu, J. C., Moyse, E. and Duchamp, A. (1997). Dopaminergic modulation of mitral cell activity in the frog olfactory bulb: a combined radioligand binding–electrophysiological study. Neurosci. 79(1): 203-216.

Euronews and Reuters (2022). Rodents to the rescue: Trained rats with hi-tech backpacks could save your life in a disaster. Biztech News. https://www.euronews.com/next/2022/11/11/rodents-to-the-rescue-trained-rats-with-hi-tech-backpacks-could-save-your-life-in-a-disast. Date accessed: January 6, 2023.

Fatola, O. I., Olaolorun, F. A., Olopade, F. E., and Olopade, J. O. (2019). Trends in vanadium neurotoxicity. Brain Res. Bull. 145: 75–80. https://doi.org/10.1016/j.brainresbull.2018.03.010

Faulogy, E. I., Kubikova, E. and Benuska, J. (2008). Microscopical structure of the hippocampus of the rat. Bratisl. Med. J. 109(3): 106-110.

Ferrer I, Fabregues I, Pineda M, Gracia I, and Ribalta T. A. (1984). Golgi study of cerebellar atrophy in human chronic alcoholism. Neuropathol. Appl. Neurobiol. 10(4): 245–253.

Folarin, O. R., Adaramoye, O. A., Akanni, O. O., and Olopade, J. O. (2018). Changes in the brain antioxidant profile after chronic vanadium administration in mice. Metab. Brain Dis. 33(2): 377–385. https://doi.org/10.1007/s11011-017-0070-9

Folarin, O. R., Snyder, A. M., Peters, D. G., Olopade, F., Connor, J. R., and Olopade, J. O. (2017). Brain Metal Distribution and Neuro-Inflammatory Profiles after Chronic Vanadium Administration and Withdrawal in Mice. Front. Neuroanat. 11:58. https://doi.org/10.3389/fnana.2017.00058

Garcia, G. B., Biancardi, M. E., and Quiroga, A. D. (2005). Vanadium (V)-induced neurotoxicity in the rat central nervous system: a histo-immunohistochemical study. Drug Chem. Toxicol. 28(3): 329–344. https://doi.org/10.1081/dct-200064496

Hagino-Yamagishi and Kimiko (2008). Diverse Systems for Pheromone Perception: Multiple Receptor Families in Two Olfactory Systems. Zool. Sci. 25(12): 1179–1189. https://doi.org/10.2108/zsj.25.1179

Haider S. S., Abdel-Gayoum A. A., el-Fakhri M. and Ghwarsha K. M. (1998). Effect of selenium on vanadium toxicity in different regions of rat brain. Hum. Exp. Toxicol. 17: 23–28. https://doi.org/10.1191/096032798678907784

Halász, N., Johansson, O., Hökfelt, T., Ljungdahl, Å. and Goldstein, M. (1981). Immunohistochemical identification of two types of dopamine neuron in the rat olfactory bulb as seen by serial sectioning. J. Neurocytol. 10(2): 251-259.

Hegarty, J. P., 2nd, Pegoraro, L. F. L., Lazzeroni, L. C., Raman, M. M., Hallmayer, J. F., Monterrey, J. C., Cleveland, S. C., Wolke, O. N., Phillips, J. M., Reiss, A. L., and Hardan, A. Y. (2020). Genetic and environmental influences on structural brain measures in twins with autism spectrum disorder. Mol. Psychiatry 25(10): 2556–2566. https://doi.org/10.1038/s41380-018-0330-z

Hsia, A. Y., Vincent, J. D., and Lledo, P. M. (1999). Dopamine depresses synaptic inputs into the olfactory bulb. J. Neurophysiol. 82(2): 1082-1085.

Ibe, C. S., Onyeanusi, B. I., and Hambolu, J. O. (2014). Functional morphology of the brain of the African giant pouched rat (Cricetomys gambianus) Waterhouse, 1840). Onderstepoort. J. Vet. Res. 81(1), e1–e7. https://doi.org/10.4102/ojvr.v81i1.644

Igado, Olumayowa O.; Olopade, James O.; Adesida, Adebukola; Aina, Oluwasanmi O.; Farombi, Ebenezer O. (2012). Morphological and biochemical investigation into the possible neuroprotective effects of kolaviron (Garcinia kola bioflavonoid) on the brains of rats exposed to vanadium. Drug Chem. Toxicol. 35(4): 371–380. https://doi.org/10.3109/01480545.2011.630005

Johnston, R. E. (2000). Chemical communication and pheromones: the types of chemical signals and the role of the vomeronasal system. Neurobiol. Taste Smell 2:101-127.

Jyothi, N. R. (2020). Heavy Metal Sources and Their Effects on Human Health. In M. K. Nazal, & H. Zhao (Eds.), Heavy Metals - Their Environmental Impacts and Mitigation. IntechOpen. https://doi.org/10.5772/intechopen.95370

Jennett, W. B. (1968). Blood flow techniques in clinical neurosurgery. In: Bain, W. H. and Harper, A. M. (eds). Blood flow through organs and tissues. E. S. Livingston Ltd., Edinburg, pp 349 - 354.

Kano M and Watanabe M (2020). Cerebellar circuits: Chapter 4. In: John Rubenstein, Pasko Rakic, Bin Chen, Kenneth Y. Kwan (eds). Neural Circuit and Cognitive Development (Second Edition), Academic Press. pp 79-102. https://doi.org/10.1016/B978-0-12-814411-4.00004-4.

Kemp, K.C., Cook, A.J., Redondo, J., Kurian, K. M., Scolding, N. J., and Wilkins, A. (2016). Purkinje cell injury, structural plasticity and fusion in patients with Friedreich’s ataxia. Acta Neuropathol. Commun. 4:53. https://doi.org/10.1186/s40478-016-0326-3

Koster, N. L., Norman, A. B., Richtand, N. M., Nickell, W. T., Puche, A. C., Pixley, S. K., and Shipley, M. T. (1999). Olfactory receptor neurons express D2 dopamine receptors. J. Comp. Neurol. 411(4): 666-673.

Pyrzyńska K. and Wierzbicki T. (2004). Determination of vanadium species in environmental samples. Talanta. 64(4): 823–829. https://doi.org/10.1016/j.talanta.2004.05.007

Lang-Ouellette, D., Gruver, K.M., Smith-Dijak, A. Blot, F. G. C., Stewart, C. A., de Vanssay de Blavous, P., Li, C. H., Van Eitrem, C., Rosen, C., Faust, P. L., Schonewille, M., and Watt, A. J. (2021). Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function. Nat. Commun. 12(1): 4129. https://doi.org/10.1038/s41467-021-24390-4

Li, B., Xia, M., Zorec, R., Parpura, V., and Verkhratsky, A. (2021). Astrocytes in heavy metal neurotoxicity and neurodegeneration. Brain Res. 1752:147234. https://doi.org/10.1016/j.brainres.2020.147234

Li H., Zhou D. Zhang Q., Feng C., Zheng W., He K. and Lan Y. (2013). Vanadium exposure-induced neurobehavioral alterations among Chinese workers. Neurotoxicology 36:49–54. https://doi.org/10.1016/j.neuro.2013.02.008

Louis, E. D., Lee, M., Babij, R., Ma, K., Cortés, E., Vonsattel, J. P., and Faust, P. L. (2014). Reduced Purkinje cell dendritic arborization and loss of dendritic spines in essential tremor. Brain, 137(12): 3142–3148. https://doi.org/10.1093/brain/awu314

Makoye K. (2022). Giant rats help scientists in Tanzania trying to snuff out tuberculosis. https://www.aa.com.tr/en/africa/giant-rats-help-scientists-in-tanzania-trying-to-snuff-out-tuberculosis/2466694. Data accessed: January 3, 2023.

Mavroudis, I. A., Manani, M. G., Petrides, F., Petsoglou, K., Njau, S. D., Costa, V. G., and Baloyannis, S. J. (2013). Dendritic and spinal pathology of the Purkinje cells from the human cerebellar vermis in Alzheimer's disease. Psychiatr Danub. 25: 221–226.

Milardi, D., Quartarone, A., Bramanti, A., Anastasi, G., Bertino, S., Basile, G. A., Buonasera, P., Pilone, G., Celeste, G., Rizzo, G., Bruschetta, D., and Cacciola, A. (2019). The Cortico-Basal Ganglia-Cerebellar Network: Past, Present and Future Perspectives. Front. Syst. Neurosci. 13: 61. https://doi.org/10.3389/fnsys.2019.00061

Musser G. G. and Carleton M. D. (2005). Family Muridae. In: Wilson DE, Reeder DM, (eds). Mammal species of the world: a taxonomic and geographic reference. Baltimore: The Johns Hopkins University Press. pp 745–752.

Mustapha O.A., Awala-Ajakaiye M., Taiwo B., Bello S. T., Olude M. A., and Olopade J. O. (2023). Vanadium impairs neuronal infrastructure of the hippocampal trisynaptic loop in the African Giant Rat (Cricetomys gambianus, Waterhouse). Nig. J. Neurosci. 14(1):1-9. http://doi.org/10.47081/njn2023.14.1/001

Mustapha O. A., Ayoade O. E., Ogunbunmi T. K., and Olude M. A. (2015). Morphology of the oral cavity of the African giant rat (Cricetomys gambianus, Waterhouse). Bulg. J. Vet. Med. 18(1): 19-30.

Mustapha O.A., Olude M.A., Bello S.T., Taiwo A, Jagun A., and Olopade J.O. (2018). Peripheral axonopathy in sciatic nerve of adult Wistar rats following exposure to vanadium. J. Peripher. Nerv. Syst. 24(1): 94-99. https://doi.org/10.1111/jns.12294.

Mustapha O.A., Olude M.A., Taiwo B., and Olopade J.O. (2019). Cytoarchitecture of the Hippocampal Formation in the African Giant Rat (Cricetomys gambianus, Waterhouse). Niger. J. Physiol. Sci. 34: 55-62.

Mustapha, O. A., Oke, B., Offen, N., Siren, A. L. and Olopade, J. O. (2014). Neurobehavioral and cytotoxic effects of vanadium during oligodendrocyte maturation: a protective role for erythropoietin. Environ. Toxicol. Pharmacol. 38(1): 98–111. doi: 10.1016/j.etap.2014.05.001.

Naga R.S.S.S. (2021). Anatomy of Cerebellum. In (Ed.), Spinocerebellar Ataxia - Concepts, Particularities and Generalities. IntechOpen. https://doi.org/10.5772/intechopen.97579

Naseri, K., Tahergorabi, Z., Khazdair, M. R., and Sadeghi, M. (2021). Toxic Mechanisms of Five Heavy Metals: Mercury, Lead, Chromium, Cadmium, and Arsenic. Front. Pharmacol. https://doi.org/10.3389/fphar.2021.643972

Ngwa, H. A., Kanthasamy, A., Jin, H., Anantharam, V., and Kanthasamy, A. G. (2014). Vanadium Exposure Induces Olfactory Dysfunction in an Animal Model of Metal Neurotoxicity. Neurotoxicology, 43: 73. https://doi.org/10.1016/j.neuro.2013.12.004

Olaolorun, F. A., Olopade, F. E., Usende, I. L., Lijoka, A. D., Ladagu, A. D., and Olopade, J. O. (2021). Neurotoxicity of vanadium. Adv. Neurotoxicol. 299–327. https://doi.org/10.1016/bs.ant.2021.01.002

Olayemi A., Nicolas V., Hulselmans J., Missoup A.D., Fichet-Calvet E., Amundala D., Dudu A., Dierckx T., Wendelen W., Leirs H., and Verheyen E. (2012). Taxonomy of The African Giant Pouched Rats (Nesomyidae: Cricetomys): Molecular and Craniometric Evidence Support An Unexpected High Species Diversity. Zool. J. Linn. Soc. 165(3): 700–719. https://doi.org/10.1111/j.1096-3642.2012.00823.x

Olude M. A., Mustapha O. A. and Olopade J. O. (2016). Morphological characterization of the African giant rat (cricetomys gambianus, waterhouse) brain across age groups: gross features of cortices. Niger. J. Physiol. Sci. 31: 133-138.

Olude, M. A., Ogunbunmi, T. K., Olopade, J. O., and Ihunwo, A. O. (2014). The olfactory bulb structure of African giant rat (Cricetomys gambianus, Waterhouse 1840) I: cytoarchitecture. Anat. Sci. Int. 89(4): 224–231. https://doi.org/10.1007/s12565-014-0227-0

Poling A., Mahoney A., Beyene N., Mgode G., Weetjens B., Cox C., and Durgin A. (2015). Using giant african pouched rats to detect human tuberculosis: a review. Pan Afr. Med. J. 21:333. doi: 10.11604/pamj.2015.21.333.2977

Poling, A., Weetjens, B., Cox, C., Beyene, N., Durgin, A. and Mahoney, A. (2011). Tuberculosis Detection by Giant African Pouched Rats. Behav. Anal. 34(1): 47-54. https://doi.org/10.1007/BF03392234

Purves D, Augustine GJ, Fitzpatrick D, et al., editors. Neuroscience. 2nd edition. Sunderland (MA): Sinauer Associates; 2001. Circuits within the Cerebellum. Available from: https://www.ncbi.nlm.nih.gov/books/NBK10865/

Redondo, J., Kemp, K., Hares, K., Rice, C., Scolding, N., and Wilkins, A. (2015). Purkinje Cell Pathology and Loss in Multiple Sclerosis Cerebellum. Brain Pathol. (Zurich, Switzerland), 25(6): 692–700. https://doi.org/10.1111/bpa.12230

Rey, N. L., Wesson, D. W., and Brundin, P. (2018). The olfactory bulb as the entry site for prion-like propagation in neurodegenerative diseases. Neurobiol. Dis. 109: 226-248. https://doi.org/10.1016/j.nbd.2016.12.013

Rojas-Lemus, M., Bizarro-Nevares, P., López-Valdez, N., González-Villalva, A., Guerrero-Palomo, G., Cervantes-Valencia, M. E. , Tavera-Cabrera, O., Rivera-Fernández, N., Casarrubias-Tabarez, B., Ustarroz-Cano, M., Rodríguez-Zepeda, A., Pasos-Nájera, F., and Goes, T. F. d. (2020). Oxidative Stress and Vanadium. In S. Soloneski, & M. L. Larramendy (Eds.), Genotoxicity and Mutagenicity - Mechanisms and Test Methods. IntechOpen. https://doi.org/10.5772/intechopen.90861

Roos W. P. and Kaina B. (2006). DNA damage-induced cell death by apoptosis. Trends Mol. Med. 12: 440–450.

Ścibior, A., and Kurus, J. (2019). Vanadium and Oxidative Stress Markers - In Vivo Model: A Review. Curr. Med. Chem. 26(29): 5456–5500. https://doi.org/10.2174/0929867326666190108112255

Shintaku M, and Kaneda D. (2009). Chromosome 16q22.1-linked autosomal dominant cerebellar ataxia: an autopsy case report with some new observations on cerebellar pathology. Neuropathol. 29: 285–292.

Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., and Sutton, D. J. (2011). Heavy Metals Toxicity and the Environment. EXS 101:133. https://doi.org/10.1007/978-3-7643-8340-4_6

Thau L, Reddy V, and Singh P. (2022). Anatomy, Central Nervous System. [Updated 2022 Oct 10]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK542179/

Tole, S., and Hébert, J. (2013). Telencephalon Patterning. Patterning and Cell Type Specification in the Developing CNS and PNS. Editors: John Rubenstein, Pasko Rakic (1st eds). Comprehensive Developmental Neuroscience, pp 3-24. https://doi.org/10.1016/B978-0-12-397265-1.00018-6

Tufo, C., Poopalasundaram, S., Dorrego-Rivas, A., Ford, M. C., Graham, A., and Grubb, M. S. (2022). Development of the mammalian main olfactory bulb. Development. 149(3): dev200210. doi: 10.1242/dev.200210

Usende, I. L., Alimba, C. G., Emikpe, B. O., Bakare, A. A., and Olopade, J. O. (2018). Intraperitoneal sodium metavanadate exposure induced severe clinicopathological alterations, hepato-renal toxicity and cytogenotoxicity in African giant rats (Cricetomys gambianus, Waterhouse, 1840). Environ. Sci. Pollut. Res. 25(26): 26383–26393. https://doi.org/10.1007/s11356-018-2588-8

Usende, I. L., Olopade, J. O., Azeez, I. A., Andrioli, A., Bankole, M. O., Olopade, F. E., Nafady, A. A., and Bentivoglio, M. (2022). Neuroecotoxicology: Effects of environmental heavy metal exposure on the brain of African giant rats and the contribution of vanadium to the neuropathology. IBRO Neurosci. Reports, 13: 215–234. https://doi.org/10.1016/j.ibneur.2022.08.008

van der Heijden, M. E., and Sillitoe, R. V. (2021). Interactions between Purkinje cells and granule cells coordinate the development of functional cerebellar circuits. Neuroscience, 462:4. https://doi.org/10.1016/j.neuroscience.2020.06.010

White, J. J., Arancillo, M., Stay, T. L., George-Jones, N. A., Levy, S. L., Heck, D. H., & Sillitoe, R. V. (2014). Cerebellar Zonal Patterning Relies on Purkinje Cell Neurotransmission. J. Neurosci. 34 (24):8231-8245. https://doi.org/10.1523/JNEUROSCI.0122-14.2014

White, J. J., Bosman, L. W. J., Blot, F. G. C., Osório, C., Kuppens, B. W., Krijnen, W. H. J. J., Andriessen, C., De Zeeuw, C. I., Jaarsma, D., and Schonewille, M. (2021). Region-specific preservation of Purkinje cell morphology and motor behavior in the ATXN1[82Q] mouse model of spinocerebellar ataxia 1. Brain Pathol. (Zurich, Switzerland), 31(5): e12946. https://doi.org/10.1111/bpa.12946

Xia, G., McFarland, K. N., Wang, K., Sarkar, P. S., Yachnis, A. T., & Ashizawa, T. (2013). Purkinje cell loss is the major brain pathology of spinocerebellar ataxia type 10. J. Neurol. Neurosurg. Psychiatry, 84(12): 1409–1411. https://doi.org/10.1136/jnnp-2013-305080

Xiong, Z., Xing, C., Xu, T., Yang, Y., Liu, G., Hu, G., Cao, H., Zhang, C., Guo, X., and Yang, F. (2021). Vanadium Induces Oxidative Stress and Mitochondrial Quality Control Disorder in the Heart of Ducks. Front. Vet. Sci. 8: 756534. https://doi.org/10.3389/fvets.2021.756534

Yan, X., Joshi, A., Zang, Y., Assunção, F., Fernandes, H. M., and Hummel, T. (2022). The Shape of the Olfactory Bulb Predicts Olfactory Function. Brain Sci. 12(2): https://doi.org/10.3390/brainsci12020128

Zhao Y., Ye L., Liu H., Xia Q., Zhang Y., Yang X., and Wang K. (2010). Vanadium compounds induced mitochondria permeability transition pore (PTP) opening related to oxidative stress. J. Inorg. Biochem. 104: 371–378.

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