{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,16]],"date-time":"2026-04-16T12:16:11Z","timestamp":1776341771501,"version":"3.51.2"},"reference-count":137,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2025,11,17]],"date-time":"2025-11-17T00:00:00Z","timestamp":1763337600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Zhirmunsky National Scientific Center of Marine Biology (NSCMB) FEB RAS","award":["121082600034-5"],"award-info":[{"award-number":["121082600034-5"]}]}],"content-domain":{"domain":["www.mdpi.com"],"crossmark-restriction":true},"short-container-title":["IJMS"],"abstract":"<jats:p>Currently, the problem of climate change on Earth is becoming increasingly urgent. These changes are the reason for the increasingly pronounced adaptive differences in different species of fish. A significant gap in ultrastructural data on the organization of the salmon cerebellum was the main motivation for this study\u2019s microscopic and ultrastructural analyses using transmission and scanning electron microscopy of the cerebellum of juvenile chum salmon Oncorhynchus keta. The study of the interneuron composition of the cerebellum showed the presence of stellate cells in the molecular layer, projection Purkinje cells, and eurydendroid cells in the ganglion layer. Large Golgi cells and granular cells were found in the granular layer. The study of the synaptic structure of the molecular layer showed the presence of synaptic contacts of electrotonic and chemical types, which are an important link in interneuronal communications. Most synaptic endings of parallel fibers of the excitatory type in juvenile chum salmon converge onto dendrites of Purkinje cells. Transmission electron microscopy (TEM) study of neuro\u2013glial relationships also revealed a heterogeneous population of astrocytes and microglia in the cerebellum of juvenile chum salmon. Patterns of apoptosis and phagocytosis involving protoplasmic astrocytes were detected. The presence of protoplasmic astrocytes in the cerebellum of juvenile chum salmon contrasts with data reported for zebrafish. The conducted studies allow us to conclude that the homeostatic growth of the cerebellum of juvenile chum salmon can occur according to an uncertain pattern and be mediated by the presence of adult-type neural stem\/progenitor cells (aNSPCs). The presence of aNSPCs of glial and non-glial types in the cerebellum of juvenile chum salmon was demonstrated by TEM and scanning electron microscopy (SEM). The discovery of a large population of non-glial aNSPCs in the dorsal matrix zone (DMZ) and granular layer of juvenile chum salmon, as well as stromal cell clusters on the surface of the cerebellar molecular layer, suggests the activity of a neurogenic program in the brain of juvenile chum salmon that is mainly active during embryonic stages in other vertebrate species. The phenomenon of embryonization in the cerebellum of juvenile chum salmon is determined by the presence of non-glial aNSPCs, which contribute to homeostatic growth.<\/jats:p>","DOI":"10.3390\/ijms262211123","type":"journal-article","created":{"date-parts":[[2025,11,18]],"date-time":"2025-11-18T09:58:42Z","timestamp":1763459922000},"page":"11123","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Ultrastructural Characteristics of the Juvenile Chum Salmon (Oncorhynchus keta) Cerebellum: Interneuron Composition, Neuro\u2013Glial Interactions, Homeostatic Neurogenesis, and Synaptic Plasticity"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0388-3147","authenticated-orcid":false,"given":"Evgeniya","family":"Pushchina","sequence":"first","affiliation":[{"name":"A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 690041 Vladivostok, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Evgeniya","family":"Vekhova","sequence":"additional","affiliation":[{"name":"A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 690041 Vladivostok, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eugenia","family":"Pimenova","sequence":"additional","affiliation":[{"name":"A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 690041 Vladivostok, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna","family":"Akhmadieva","sequence":"additional","affiliation":[{"name":"Research and Manufacturing Company \u201cHome of Pharmacy\u201d, 245, Zavodskaya St., Kuzmolovskiy t.s., Vsevolozhsk District, Leningrad Oblast, 188663 Saint Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mariya","family":"Bykova","sequence":"additional","affiliation":[{"name":"A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 690041 Vladivostok, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,11,17]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1002\/cne.903160103","article-title":"Distribution of zebrin II in the gigantocerebellum of the mormyrid fish Gnathonemus petersii compared with other teleosts","volume":"316","author":"Meek","year":"1992","journal-title":"J. Comp. Neurol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1002\/cne.20979","article-title":"Afferent and efferent connections of the cerebellum of a salmonid, the rainbow trout (Oncorhynchus mykiss): A tract-tracing study","volume":"497","author":"Folgueira","year":"2006","journal-title":"J. Comp. Neurol."},{"key":"ref_3","first-page":"1","article-title":"Comparative anatomy of the cerebellum","volume":"Volume 25","author":"Fox","year":"1967","journal-title":"Progress in Brain Research"},{"key":"ref_4","unstructured":"Herleif, M. (2018). Neural stem cells in the cerebellum of juvenile masu salmon (Oncorhynchus masu) arter mechanical inhury. Teleost: Physiology, Evolution and Classification, Nava Science Publisher, Inc."},{"key":"ref_5","unstructured":"Northcutt, R.G., and Davis, R.E. (1983). Organization of the teleost cerebellum. Fish Neurobiology, University of Michigan Press."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1002\/cne.21809","article-title":"Morphological analysis of the mormyrid cerebellum using immunohistochemistry with emphasis on the unusual neuronal organization of the valvula","volume":"519","author":"Meek","year":"2008","journal-title":"J. Comp. Neurol."},{"key":"ref_7","unstructured":"Llin\u00e1s, R. (1969). A survey of the general morphology, the fiber connections, and the possible significance of gigantocerebellum of mormyrid fishes. Neurobiology of Cerebellar Evolution and Development, American Medical Association."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Pushchina, E., Bykova, M.E., Vekhova, E.E., and Pimenova, E.A. (2025). Immunohistochemical and ultrastructural analysis of adult neurogenesis involving glial and non-glial progenitors in the cerebellum of juvenile chum salmon Oncorhynchus keta. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms26199267"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1002\/cne.902560413","article-title":"Morphology and distribution of the projection neurons in the cerebellum in a teleost, Sebastiscus marmoratus","volume":"256","author":"Murakami","year":"1987","journal-title":"J. Comp. Neurol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1007\/BF00569848","article-title":"On the development of the cerebellum of the trout Salmo gairdneri. III. Development of neuronal elements","volume":"153","author":"Pouwels","year":"1978","journal-title":"Anat. Embryol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/BF00569849","article-title":"On the development of the cerebellum of the trout Salmo gairdneri. IV. Development of the pattern of connectivity","volume":"153","author":"Pouwels","year":"1978","journal-title":"Anat. Embryol."},{"key":"ref_12","unstructured":"Llin\u00e1s, R. (1969). Fine structural studies of the cerebellar cortex in a mormyrid fish. Neurobiology of Cerebellar Evolution and Development, American Medical Association."},{"key":"ref_13","unstructured":"Pushchina, E.V., Varaksin, A.A., Shukla, S., and Obukhov, D.K. (2017). The Neurochemical Organization and Adult Neurogenesis in the Masu Salmon Brain, Nova Science Pub Inc."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Pushchina, E.V., and Varaksin, A.A. (2024). Constitutive neurogenesis and neuronal plasticity in the adult cerebellum and brainstem of rainbow trout, Oncorhynchus mykiss. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25115595"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1134\/S1062360417050071","article-title":"GFAP and PCNA marking in the cerebellum of masu salmon\u1fbfs (Oncorhynchus masou) juvenile after mechanical injury","volume":"48","author":"Stukaneva","year":"2017","journal-title":"Rus. J. Dev. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Pushchina, E.V., Stukaneva, M.E., and Varaksin, A.A. (2020). Hydrogen sulfide modulates adult and reparative neurogenesis in the cerebellum of juvenile masu salmon, Oncorhynchus masou. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21249638"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Pushchina, E.V., Bykova, M.E., and Varaksin, A.A. (2024). Post-traumatic expressions of aromatase B, glutamine synthetase, and cystathionine-beta-synthase in the cerebellum of juvenile chum salmon, Oncorhynchus keta. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25063299"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1023\/A:1015867808459","article-title":"Morphological organization of large Golgi neurons in the cerebellum of the opisthocentrid Pholidapus dybowskii","volume":"32","author":"Pushchina","year":"2002","journal-title":"Neurosci. Behav. Physiol."},{"key":"ref_19","first-page":"437","article-title":"Argyrophilic and nitroxydergic bipolar neurons (Lugaro cells) in the cerebellum of Pholidapus dybowskii","volume":"37","author":"Pushchina","year":"2001","journal-title":"Zh. Evol. Biokhim. Fiziol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1002\/cne.903060111","article-title":"Palisade pattern of mormyrid Purkinje cells. A correlated light and electron microscopic study","volume":"306","author":"Meek","year":"1991","journal-title":"J. Comp. Neurol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1002\/cne.903240311","article-title":"Afferents to the oculomotor nucleus in the goldfish (Carassius auratus) as revealed by retrograde labeling with horseradish peroxidase","volume":"324","author":"Torres","year":"1992","journal-title":"J. Comp. Neurol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1002\/cne.20553","article-title":"Morphology and immunohistochemistry of efferent neurons of the goldfish corpus cerebelli","volume":"487","author":"Ikenaga","year":"2005","journal-title":"J. Comp. Neurol."},{"key":"ref_23","unstructured":"Llin\u00e1s, R. (1969). Aspects of the histology of the cerebellum of mormyrid fishes. Neurobiology of Cerebellar Evolution and Development, American Medical Association."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1007\/BF00522813","article-title":"The neuronal organization of cerebellar lobe C1 in the mormyrid fish Gnathonemus petersii (Teleostei)","volume":"144","author":"Nieuwenhuys","year":"1974","journal-title":"Z. Anat-Entwickl. Gesch."},{"key":"ref_25","first-page":"581","article-title":"Distribution of cholineacetyltransferase histochemistry in isthmus and medulla of Onchorynchus masou. Tract-tracing observation on the ascending meso-pontine cholinergic system","volume":"49","author":"Pushchina","year":"2007","journal-title":"Tsitologiia"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/S0165-3806(98)00085-6","article-title":"Parvalbumin immunoreactivity during the development of the cerebellum of the rainbow trout","volume":"109","author":"Porteros","year":"1998","journal-title":"Dev. Brain Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1002\/1096-9861(20001218)428:3<450::AID-CNE5>3.0.CO;2-T","article-title":"Distribution of choline acetyltransferase (ChAT) immunoreactivity in the brain of the adult trout, and tract-tracing observations on the connections of the nuclei of the isthmus","volume":"428","year":"2000","journal-title":"J. Comp. Neurol."},{"key":"ref_28","unstructured":"Kupriyanov, V.V. (2005). Cerebellar Cortex, Nauka."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1016\/j.ydbio.2009.04.013","article-title":"Anatomy of zebrafish cerebellum and screen for mutations affecting its development","volume":"330","author":"Bae","year":"2009","journal-title":"Dev. Biol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Manto, M., Gruol, D., Schmahmann, J., Koibuchi, N., and Sillitoe, R. (2020). Cerebellar development and neurogenesis in zebrafish. Handbook of the Cerebellum and Cerebellar Disorders, Springer.","DOI":"10.1007\/978-3-319-97911-3"},{"key":"ref_31","unstructured":"Obukhov, D.K., and Andreeva, N.G. (2024). Evolutionary Morphology of the Nervous System in Vertebrates, Higher Education. [3rd ed.]. Textbook; Revised and Expanded."},{"key":"ref_32","first-page":"197","article-title":"Further observations on cerebellar climbing fibers. A study by means of light microscopy, confocal laser scanning microscopy and scanning and transmission electron microscopy","volume":"24","author":"Alvarado","year":"2000","journal-title":"Biocell"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"11846","DOI":"10.1073\/pnas.1403105111","article-title":"Functional regionalization of the teleost cerebellum analyzed in vivo","volume":"111","author":"Matsui","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2275","DOI":"10.1002\/cne.23065","article-title":"The cellular composition of neurogenic periventricular zones in the adult zebrafish forebrain","volume":"520","author":"Lindsey","year":"2012","journal-title":"J. Comp. Neurol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1007\/s11062-021-09904-6","article-title":"Constitutive neurogenesis in the brain of different vertebrate groups","volume":"52","author":"Stukaneva","year":"2020","journal-title":"Neurophysiology"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Lindsey, B.W. (2023). A Comparative view of cerebellar morphology and diversity in fishes. Development of the Cerebellum from Molecular Aspects to Diseases, Springer. Available online: https:\/\/link.springer.com\/chapter\/10.1007\/978-3-031-23104-9_8.","DOI":"10.1007\/978-3-031-23104-9_8"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Pushchina, E.V., Pimenova, E.A., Kapustyanov, I.A., and Bykova, M.E. (2025). Ultrastructural study and immunohistochemical characteristics of mesencephalic tegmentum in juvenile chum salmon (Oncorhynchus keta) brain after acute traumatic injury. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms26020644"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"York, R.A., Byrne, A.L., Abdilleh, K., Patil, C., Steelman, T., Finger, T.E., and Russell, D.F. (2019). Behavior evolution contributes to hindbrain diversification among lake malawi cichlid fish. Sci. Rep., 9.","DOI":"10.1038\/s41598-019-55894-1"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Manto, M., Gruol, D.L., Schmahmann, J., Koibuchi, N., and Rossi, F. (2013). Teleost fish. Handbook of the Cerebellum and Cerebellar Disorders, Springer.","DOI":"10.1007\/978-94-007-1333-8"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1002\/cne.20983","article-title":"Cell morphology and circuitry in the central lobes of the mormyrid cerebellum","volume":"497","author":"Han","year":"2006","journal-title":"J. Comp. Neurol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Nieuwenhuys, R., Ten Donkelaar, H.J., and Nicholson, C. (1998). The Central Nervous System of Vertebrates, Springer.","DOI":"10.1007\/978-3-642-18262-4"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Caron, A., Trzuskot, L., and Lindsey, B.W. (2022). Uncovering the spectrum of adult zebrafish neural stem cell cycle regulators. Front Cell Dev. Biol., 10.","DOI":"10.3389\/fcell.2022.941893"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.jare.2023.08.013","article-title":"Distribution, contribution and regulation of nestin+ cells","volume":"61","author":"Tong","year":"2024","journal-title":"J. Adv. Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1007\/s00018-023-04879-5","article-title":"Development, circuitry, and function of the zebrafish cerebellum","volume":"80","author":"Schramm","year":"2023","journal-title":"Cell Mol. Life Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ydbio.2014.09.030","article-title":"Establishment of Gal4 transgenic zebrafish lines for analysis of development of cerebellar neural circuitry","volume":"397","author":"Takeuchi","year":"2015","journal-title":"Dev. Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1111\/j.1749-6632.2002.tb07574.x","article-title":"Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning","volume":"978","author":"Ito","year":"2002","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1038\/nrn962","article-title":"The molecular organization of cerebellar long-term depression","volume":"3","author":"Ito","year":"2002","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1016\/j.pneurobio.2006.02.006","article-title":"Cerebellar circuitry as a neuronal machine","volume":"78","author":"Ito","year":"2006","journal-title":"Prog. Neurobiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1007\/BF00188547","article-title":"Parvalbumin.immunoreactive neurons and fibres in the teleost cerebellum","volume":"185","author":"Alonso","year":"1992","journal-title":"Anat. Embryol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"17330","DOI":"10.1073\/pnas.2005633117","article-title":"Functionally distinct Purkinje cell types show temporal precision in encoding locomotion","volume":"117","author":"Chang","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3711","DOI":"10.1016\/j.cub.2018.09.060","article-title":"Cellular-resolution imaging of vestibular processing across the larval zebrafish brain","volume":"28","author":"Vanwalleghem","year":"2018","journal-title":"Curr. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1002\/cne.20571","article-title":"Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain","volume":"488","author":"Zupanc","year":"2005","journal-title":"J. Comp. Neurol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1002\/ar.21291","article-title":"Neurogenesis in the adult goldfish cerebellum","volume":"294","author":"Delgado","year":"2011","journal-title":"Anat. Rec."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"3471","DOI":"10.1002\/cne.23100","article-title":"Characterization of cell proliferation throughout the brain of the African cichlid fish Astatotilapia burtoni and its regulation by social status","volume":"520","author":"Maruska","year":"2012","journal-title":"J. Comp. Neurol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1111\/j.1474-9726.2011.00781.x","article-title":"Adult neurogenesis in the short-lived teleost Nothobranchius furzeri: Localization of neurogenic niches, molecular characterizing and effects of aging","volume":"11","author":"Tozzini","year":"2012","journal-title":"Aging Cell"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.brainres.2010.01.045","article-title":"Proliferation zones in adult medaka (Oryzias latipes) brain","volume":"1323","author":"Kuroyanagi","year":"2010","journal-title":"Brain Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1002\/cne.903530205","article-title":"Proliferation zones in the brain of adult gymnotiform fish: A quantitative mapping study","volume":"353","author":"Zupanc","year":"1995","journal-title":"J. Comp. Neurol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Feliciano, D.M., Bordey, A., and Bonfanti, L. (2015). Noncanonical sites of adult neurogenesis in the mammalian brain. Cold Spring Harb. Perspect. Biol., 7.","DOI":"10.1101\/cshperspect.a018846"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Pushchina, E.V., Kapustyanov, I.A., and Kluka, G.G. (2024). Adult neurogenesis of teleost fish determines high neuronal plasticity and regeneration. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25073658"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Pushchina, E.V., Varaksin, A.A., and Obukhov, D.K. (2022). Molecular markers of adult neurogenesis in the telencephalon and tectum of rainbow trout. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23031188"},{"key":"ref_61","unstructured":"Mommsen, T.P. (1998). Growth and Metabolism, CRC."},{"key":"ref_62","first-page":"R1327","article-title":"Zebrafish and giant danio models for muscle growth: Determinate vs. indeterminate growth as determined by morphometric analysis","volume":"291","author":"Biga","year":"2006","journal-title":"Am. J. Phys. Regul. Integr. Comp. Phys."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"6142","DOI":"10.1523\/JNEUROSCI.0072-09.2009","article-title":"Stem cells in the adult zebrafish cerebellum: Initiation and maintenance of a novel stem cell niche","volume":"29","author":"Kaslin","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.ydbio.2006.03.040","article-title":"Neural stem cells and neurogenesis in the adult zebrafish brain: Origin, proliferation dynamics, migration and cell fate","volume":"295","author":"Grandel","year":"2006","journal-title":"Dev. Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"3591","DOI":"10.1111\/ejn.12729","article-title":"Sensory-specific modulation of adult neurogenesis in sensory structures is associated with the type of stem cell present in the neurogenic niche of the zebrafish brain","volume":"40","author":"Lindsey","year":"2014","journal-title":"Eur. J. Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Zupanc, G.K.H. (2021). Adult neurogenesis in the central nervous system of teleost fish: From stem cells to function and evolution. J. Exp. Biol., 224.","DOI":"10.1242\/jeb.226357"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1016\/j.neuron.2011.05.001","article-title":"Adult neurogenesis in the mammalian brain: Significant answers and significant questions","volume":"70","author":"Ming","year":"2011","journal-title":"Neuron"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1002\/dneu.22183","article-title":"Changes in the social environment induce neurogenic plasticity predominantly in niches residing in sensory structures of the zebrafish brain independently of cortisol levels","volume":"74","author":"Lindsey","year":"2014","journal-title":"Dev. Neurobiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.cub.2010.11.049","article-title":"A High proliferation rate is required for cell reprogramming and maintenance of human embryonic stem cell identity","volume":"21","author":"Sergio","year":"2011","journal-title":"Curr. Biol."},{"key":"ref_70","first-page":"957","article-title":"Repeated ecological and life cycle transitions make salamanders an ideal model for evolution and development","volume":"251","author":"Bonett","year":"2022","journal-title":"Dev. Dyn. Off. Publ. Am. Assoc. Anat."},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Bruce, R.C. (2013). Size-mediated tradeoffs in life-history traits in dusky salamanders. Copeia, 262\u2013267.","DOI":"10.1643\/CE-12-120"},{"key":"ref_72","first-page":"20201474","article-title":"Correlated and decoupled evolution of adult and larval body size in frogs","volume":"287","author":"Phung","year":"2020","journal-title":"Proc. Roy. Soc."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"e12757","DOI":"10.1111\/acel.12757","article-title":"The African turquoise killifish: A research organism to study vertebrate aging and diapause","volume":"17","author":"Brunet","year":"2018","journal-title":"Aging Cell"},{"key":"ref_74","unstructured":"Rodr\u00edguez-Moldes, I. (2025, November 07). Brain and nervous system functional morphology of the brains of cartilaginous fishes. Encycl. Fish Physiol., Available online: https:\/\/www.sciencedirect.com\/science\/article\/abs\/pii\/B9780123745538000046?via%3Dihub."},{"key":"ref_75","first-page":"1","article-title":"A developmental study of the cerebellar nucleus in the catshark, a basal gnathostome","volume":"89","author":"Candal","year":"2017","journal-title":"Brain Behav. Evol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1002\/cne.10629","article-title":"Afferent and efferent connections of the cerebellum of the chondrostean Acipenser baeri: A carbocyanine dye (DiI) tracing study","volume":"460","author":"Huesa","year":"2003","journal-title":"J. Comp. Neurol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1002\/cne.25271","article-title":"Morphological analysis of the cerebellum and its efferent system in a basal actinopterygian fish, Polypterus senegalus","volume":"530","author":"Ikenaga","year":"2022","journal-title":"J. Comp. Neurol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1007\/s11062-011-9192-6","article-title":"Hydrogen sulfide-, parvalbumin-, and GABA-producing systems in the masu salmon brain","volume":"43","author":"Puschina","year":"2011","journal-title":"Neurophysiology"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/0301-0082(91)90022-S","article-title":"Development of the cerebellum and its extracerebellar Purkinje cell projection in teleost fishes as determined by zebrin II immunocytochemistry","volume":"37","author":"Lannoo","year":"1991","journal-title":"Prog. Neurobiol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1159\/000113346","article-title":"Anti-zebrin II immunopositivity in the cerebellum and octavolateral nuclei in two species of stingrays","volume":"50","author":"Puzdrowski","year":"1997","journal-title":"Brain Behav. Evol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1691","DOI":"10.1007\/s00429-015-0998-7","article-title":"Morphogenesis of the cerebellum and cerebellum-related structures in the shark Scyliorhinus canicula: Insights on the ground pattern of the cerebellar ontogeny","volume":"221","author":"Candal","year":"2016","journal-title":"Brain Struct. Funct."},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Chang, W., Pedroni, A., K\u00f6ster, R.W., Giacomello, S., and Ampatzis, K. (2021). Purkinje cells located in the adult zebrafish valvula cerebelli exhibit variable functional responses. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-98035-3"},{"key":"ref_83","first-page":"111","article-title":"Induction of apoptotic activity in case of mechanical damage to the mecencephalic tegmentum of juvenile chum salmon Oncorhynchus keta","volume":"12","author":"Kapustyanov","year":"2017","journal-title":"Genes Cells"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1007\/s00441-016-2548-x","article-title":"Apoptosis in fish: Environmental factors and programmed cell death","volume":"368","author":"Adineh","year":"2017","journal-title":"Cell Tissue Res."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1080\/01926230701320337","article-title":"Apoptosis: A review of programmed cell death","volume":"35","author":"Elmore","year":"2007","journal-title":"Toxicol. Pathol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1159\/000071958","article-title":"Spatio-temporal distribution of microglia\/macrophages during regeneration in the cerebellum of adult teleost fish, Apteronotus leptorhynchus: A quantitative analysis","volume":"62","author":"Zupanc","year":"2003","journal-title":"Brain Behav. Evol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1002\/dneu.20656","article-title":"Apoptotic cell death, long-term persistence, and neuronal differentiation of aneuploid cells generated in the adult brain of teleost fish","volume":"68","author":"Rajendran","year":"2008","journal-title":"Dev. Neurobiol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1867","DOI":"10.4103\/1673-5374.280320","article-title":"GFAP expression in the optic nerve and increased H2S generation in the integration centers of the rainbow trout (Oncorhynchus mykiss) brain after unilateral eye injury","volume":"15","author":"Pushchina","year":"2020","journal-title":"Neural Regen. Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/S0006-8993(99)02339-2","article-title":"Mononuclear cell proliferation and hyperplasia during Wallerian degeneration in the visual system of the goldfish in the presence or absence of regenerating optic axons","volume":"854","author":"Ghali","year":"2000","journal-title":"Brain Res."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1002\/cne.1131","article-title":"Regenerating descending axons preferentially reroute to the gray matter in the presence of a general macrophage\/microglial reaction caudal to a spinal transection in adult zebrafish","volume":"433","author":"Becker","year":"2001","journal-title":"J. Comp. Neurol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.immuni.2016.02.013","article-title":"Microglial physiology and pathophysiology: Insights from genome-wide transcriptional profiling","volume":"44","author":"Crotti","year":"2016","journal-title":"Immunity"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"824888","DOI":"10.3389\/fnins.2022.824888","article-title":"Microglia and astrocyte function and communication: What do we know in humans?","volume":"16","author":"Garland","year":"2022","journal-title":"Front Neurosci."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1007\/s00401-009-0619-8","article-title":"Astrocytes: Biology and pathology","volume":"119","author":"Sofroniew","year":"2010","journal-title":"Acta Neuropathol."},{"key":"ref_94","doi-asserted-by":"crossref","unstructured":"Sofroniew, M.V. (2014). Astrogliosis. Cold Spring Harb. Perspect. Biol., 7.","DOI":"10.1101\/cshperspect.a020420"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1038\/s41593-020-00783-4","article-title":"Reactive astrocyte nomenclature, definitions, and future directions","volume":"24","author":"Escartin","year":"2021","journal-title":"Nat. Neurosci."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"6391","DOI":"10.1523\/JNEUROSCI.6221-11.2012","article-title":"Genomic analysis of reactive astrogliosis","volume":"32","author":"Zamanian","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1038\/nature21029","article-title":"Neurotoxic reactive astrocytes are induced by activated microglia","volume":"541","author":"Liddelow","year":"2017","journal-title":"Nature"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1152\/physrev.00041.2013","article-title":"Astrocyte reactivity and reactive astrogliosis: Costs and benefits","volume":"94","author":"Pekny","year":"2014","journal-title":"Physiol. Rev."},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Perez-Nievas, B.G., and Serrano-Pozo, A. (2018). Deciphering the astrocyte reaction in Alzheimer\u2019s disease. Front. Aging Neurosci., 10.","DOI":"10.3389\/fnagi.2018.00114"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"693851","DOI":"10.1155\/2014\/693851","article-title":"Proliferation in the alzheimer hippocampus is due to microglia, not astroglia, and occurs at sites of amyloid deposition","volume":"2014","author":"Marlatt","year":"2014","journal-title":"Neural. Plast."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1159\/000072805","article-title":"Neocortical glial cell numbers in Alzheimer\u2019s disease. A stereological study","volume":"16","author":"Pelvig","year":"2003","journal-title":"Dement. Geriatr. Cogn. Disord."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"2332","DOI":"10.1016\/j.ajpath.2013.02.031","article-title":"A phenotypic change but not proliferation underlies glial responses in Alzheimer disease","volume":"182","author":"Growdon","year":"2013","journal-title":"Am. J. Pathol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1016\/j.tins.2006.08.004","article-title":"Astrocytic complexity distinguishes the human brain","volume":"29","author":"Oberheim","year":"2006","journal-title":"Trends Neurosci."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"2285","DOI":"10.1523\/JNEUROSCI.4037-13.2014","article-title":"Phenotypic heterogeneity and plasticity of isocortical and hippocampal astrocytes in the human brain","volume":"34","author":"Sosunov","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1002\/bies.20615","article-title":"Adult neurogenesis in non-mammalian vertebrates","volume":"29","author":"Chapouton","year":"2007","journal-title":"Bioessays"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1242\/dev.122796","article-title":"A comparative view of regenerative neurogenesis in vertebrates","volume":"143","author":"Alunni","year":"2016","journal-title":"Development"},{"key":"ref_107","first-page":"193","article-title":"Teleost fish as a model system to study successful regeneration of the central nervous system","volume":"367","author":"Zupanc","year":"2013","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"6659","DOI":"10.1523\/JNEUROSCI.1717-08.2008","article-title":"Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons","volume":"28","author":"Shigetomi","year":"2008","journal-title":"J. Neurosci."},{"key":"ref_109","first-page":"102436","article-title":"Astrocytes promote ethanol-induced enhancement of intracellular Ca2+ signals through intercellular communication with neurons","volume":"24","author":"Kim","year":"2021","journal-title":"Science"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"9751","DOI":"10.1523\/JNEUROSCI.0888-20.2020","article-title":"Astrocyte-derived estrogen regulates reactive astrogliosis and is neuroprotective following ischemic brain injury","volume":"40","author":"Wang","year":"2020","journal-title":"J. Neurosci."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1007\/s11154-013-9263-7","article-title":"Estrogen, astrocytes and the neuroendocrine control of metabolism","volume":"14","author":"Lopez","year":"2013","journal-title":"Rev. Endocr. Metab. Disord."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/S0301-0082(96)00068-8","article-title":"Astrocytic neurotransmitter receptors in situ and in vivo","volume":"51","author":"Porter","year":"1997","journal-title":"Prog. Neurobiol."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.ibror.2019.08.002","article-title":"Microglial response patterns following damage to the zebrafish olfactory bulb","volume":"7","author":"Var","year":"2019","journal-title":"IBRO Rep."},{"key":"ref_114","first-page":"56014","article-title":"Modeling amyloid-\u03b242 toxicity and neurodegeneration in adult zebrafish brain","volume":"128","author":"Bhattarai","year":"2017","journal-title":"J. Vis. Exp."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1126\/science.1228773","article-title":"Acute inflammation initiates the regenerative response in the adult zebrafish brain","volume":"338","author":"Kyritsis","year":"2012","journal-title":"Science"},{"key":"ref_116","doi-asserted-by":"crossref","unstructured":"Cosacak, M.I., Papadimitriou, C., and Kizil, C. (2015). Regeneration, plasticity, and induced molecular programs in adult zebrafish brain. BioMed Res. Int., 2015.","DOI":"10.1155\/2015\/769763"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"111246","DOI":"10.1016\/j.fct.2020.111246","article-title":"Garcinol pacifies acrylamide induced cognitive impairments, neuroinflammation and neuronal apoptosis by modulating GSK signaling and activation of pCREB by regulating cathepsin B in the brain of zebrafish larvae","volume":"138","author":"Sharma","year":"2020","journal-title":"Food Chem. Toxicol."},{"key":"ref_118","doi-asserted-by":"crossref","unstructured":"Var, S.R., and Byrd-Jacobs, C.A. (2020). Role of macrophages and microglia in zebrafish regeneration. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21134768"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/nan.12011","article-title":"Review: Activation patterns of microglia and their identification in the human brain","volume":"39","author":"Boche","year":"2013","journal-title":"Neuropathol. Appl. Neurobiol."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1016\/j.neuron.2020.11.007","article-title":"Shaping neuronal fate: Functional heterogeneity of direct microglia-neuron interactions","volume":"109","year":"2021","journal-title":"Neuron"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1002\/cne.903540211","article-title":"Macrophages, microglia, and astrocytes are rapidly activated after crush injury of the goldfish optic nerve: A light and electron microscopic analysis","volume":"354","author":"Battisti","year":"1995","journal-title":"J. Comp. Neurol."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1002\/glia.23083","article-title":"Identification of a conserved and acute neurodegeneration-specific microglial transcriptome in the zebrafish","volume":"65","author":"Oosterhof","year":"2017","journal-title":"Glia"},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.expneurol.2018.04.008","article-title":"Glia maturation factor beta is required for reactive gliosis after traumatic brain injury in zebrafish","volume":"305","author":"Yin","year":"2018","journal-title":"Exp. Neurol."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1177\/42.8.8027523","article-title":"Demonstration of poly-N-acetyl lactosamine residues in ameboid and ramified microglial cells in rat brain by tomato lectin binding","volume":"42","author":"Acarin","year":"1994","journal-title":"J. Histochem. Cytochem."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/S0304-3940(99)00117-2","article-title":"Enzyme histochemical identification of microglial cells in the retina of a fish (Tinca tinca)","volume":"263","author":"Velasco","year":"1999","journal-title":"Neurosci. Lett."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1054\/tice.2001.0203","article-title":"Ultrastructural and cytochemical features of the supramedullary neurons of the pufferfish Diodon holacanthus (L.) (Osteichthyes)","volume":"33","author":"Cuoghi","year":"2001","journal-title":"Tissue Cell"},{"key":"ref_127","first-page":"231","article-title":"Microglia of teleosts: Facing a challenge in neurobiology","volume":"51","author":"Cuoghi","year":"2007","journal-title":"Eur. J. Histochem."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1111\/j.1460-9568.2007.05309.x","article-title":"Microglia-derived interleukin-6 and leukemia inhibitory factor promote astrocytic differentiation of neural stem\/progenitor cells","volume":"25","author":"Nakanishi","year":"2007","journal-title":"Eur. J. Neurosci."},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1016\/j.cell.2008.04.037","article-title":"Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo","volume":"133","author":"Peri","year":"2008","journal-title":"Cell"},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1002\/dneu.22039","article-title":"Development of ramified microglia from early macrophages in the zebrafish optic tectum","volume":"73","author":"Svahn","year":"2013","journal-title":"Dev. Neurobiol."},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1093\/brain\/awn109","article-title":"Debris clearance by microglia: An essential link between degeneration and regeneration","volume":"132","author":"Neumann","year":"2009","journal-title":"Brain J. Neurol."},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"2385","DOI":"10.1002\/glia.23477","article-title":"A limited capacity for microglial repopulation in the adult brain","volume":"66","author":"Najafi","year":"2018","journal-title":"Glia"},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1186\/s40478-016-0382-8","article-title":"Microglial neuroinflammation contributes to tau accumulation in chronic traumatic encephalopathy","volume":"4","author":"Cherry","year":"2016","journal-title":"Acta Neuropathol. Commun."},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.neulet.2015.02.004","article-title":"Live imaging reveals a new role for the sigma-1 (\u03c31) receptor in allowing microglia to leave brain injuries","volume":"591","author":"Moritz","year":"2015","journal-title":"Neurosci. Lett."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1002\/glia.22780","article-title":"Immune cell dynamics in the CNS: Learning from the zebrafish","volume":"63","author":"Oosterhof","year":"2015","journal-title":"Glia"},{"key":"ref_136","doi-asserted-by":"crossref","unstructured":"Pope, H.M., and Voigt, M.M. (2014). Peripheral glia have a pivotal role in the initial response to axon degeneration of peripheral sensory neurons in zebrafish. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0103283"},{"key":"ref_137","unstructured":"Mironov, A.A., Komissarchik, Y.Y., and Mironov, V.A. (1994). Metody Electronnoi Microscopii v biologii i Meditsine: Metodicheskoe Rukovodstvo (Methods of Electron Microscopy in Biology and Medicine: A Methodological Guide), Nauka."}],"updated-by":[{"DOI":"10.3390\/ijms27083552","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2025,11,17]],"date-time":"2025-11-17T00:00:00Z","timestamp":1763337600000}}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/22\/11123\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,16]],"date-time":"2026-04-16T10:16:24Z","timestamp":1776334584000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/22\/11123"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,17]]},"references-count":137,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2025,11]]}},"alternative-id":["ijms262211123"],"URL":"https:\/\/doi.org\/10.3390\/ijms262211123","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,17]]}}}