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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’s 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–glial 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.

In adult fish, neurogenesis occurs in many areas of the brain, including the cerebellum, with the ratio of newly formed cells relative to the total number of brain cells being several orders of magnitude greater than in mammals. Our study aimed to compare the expressions of aromatase B (AroB), glutamine synthetase (GS), and cystathionine-beta-synthase (CBS) in the cerebellum of intact juvenile chum salmon, Oncorhynchus keta. To identify the dynamics that determine the involvement of AroB, GS, and CBS in the cellular mechanisms of regeneration, we performed a comprehensive assessment of the expressions of these molecular markers during a long-term primary traumatic brain injury (TBI) and after a repeated acute TBI to the cerebellum of O. keta juveniles. As a result, in intact juveniles, weak or moderate expressions of AroB, GS, and CBS were detected in four cell types, including cells of the neuroepithelial type, migrating, and differentiated cells (graphic abstract, A). At 90 days post injury, local hypercellular areas were found in the molecular layer containing moderately labeled AroB+, GS+, and CBS+ cells of the neuroepithelial type and larger AroB+, GS+, and CBS+ cells (possibly analogous to the reactive glia of mammals); patterns of cells migration and neovascularization were also observed. A repeated TBI caused the number of AroB+, GS+, and CBS+ cells to further increase; an increased intensity of immunolabeling was recorded from all cell types (graphic abstract, C). Thus, the results of this study provide a better understanding of adult neurogenesis in teleost fishes, which is expected to clarify the issue of the reactivation of adult neurogenesis in mammalian species.

The ultrastructural organization of different cell types involved in homeostatic growth in the cerebellum of juvenile chum salmon (Oncorhynchus keta) was investigated using transmission and scanning electron microscopy. The organization of astrocytes, oligodendrocytes, dark cells, adult-type glial and non-glial progenitors, stellate neurons, and eurydendroid cells (EDCs) in the molecular and granular layers and granular eminences was characterized. The organization of dendritic bouquets of Purkinje cells and climbing fibers was studied for the first time at the ultrastructural level, and the ultrastructural features of mossy fibers and the rosettes they form were characterized. Scanning electron microscopy (SEM) revealed the presence of single and paired adult-type neural stem/progenitor cells (aNSPCs) on the cerebellar surface and stromal clusters of aNSPCs outside the dorsal matrix zone (DMZ). Immunohistochemical (IHC) verification of proliferating cell nuclear antigen (PCNA) revealed five types of proliferating cells in the cerebellum of juvenile chum salmon: neuroepithelial cells (NECs), glial aNSPCs, and non-glial aNSPCs. A glial fibrillary acidic protein-positive (GFAP) complex consisting of radial glial fibers and aNSPCs was detected in the DMZ. At the same time, a complex of GFAP+ cerebellar afferents, consisting of differentiating mossy and climbing fibers, was found to develop in the cerebellum of juvenile chum salmon. Nestin+ non-glial aNSPCs and small nestin+ resident cells were detected in the dorsal, lateral, and basal areas, as well as in the granular layer (GrL) and granular eminences (GrEm). These cell types may contribute to the homeostatic growth of the cerebellum by acting as both active participants (PCNA+) and resident (silent) aNSPCs. Studying vimentin-positive systems in the cerebellum revealed a widespread presence of proliferating glial aNSPCs that actively contribute to homeostatic growth, as well as small resident immunopositive cells throughout the cerebellum of juvenile chum salmon. Immunolocalization of the neuronal RNA-binding protein marker (HuCD) was detected in numerous molecular layer (ML) cells at the early stages of neuronal differentiation in the dorsal and lateral regions of the cerebellum of juvenile chum salmon. HuCD + EDCs were detected for the first time in the dorsal (DZ) and basal (BZ) zones, forming broad axonal arborization. Immunolabeling of HuCD in combination with transmission electron microscopy (TEM) allowed EDCs to be characterized in the cerebellum of juvenile chum salmon for the first time.

The ultrastructural organization of the nuclei of the tegmental region in juvenile chum salmon (Oncorhynchus keta) was examined using transmission electron microscopy (TEM). The dorsal tegmental nuclei (DTN), the nucleus of fasciculus longitudinalis medialis (NFLM), and the nucleus of the oculomotor nerve (NIII) were studied. The ultrastructural examination provided detailed ultrastructural characteristics of neurons forming the tegmental nuclei and showed neuro–glial relationships in them. Neurons of three size types with a high metabolic rate, characterized by the presence of numerous mitochondria, polyribosomes, Golgi apparatus, and cytoplasmic inclusions (vacuoles, lipid droplets, and dense bodies), were distinguished. It was found that large interneurons of the NFLM formed contacts with protoplasmic astrocytes. Excitatory synaptic structures were identified in the tegmentum and their detailed characteristic are provided for the first time. Microglia-like cells were found in the NIII. The ultrastructural characteristics of neurogenic zones of the tegmentum of juvenile chum salmon were also determined for the first time. In the neurogenic zones of the tegmentum, adult-type neural stem progenitor cells (aNSPCs) corresponding to cells of types III and IVa Danio rerio. In the neurogenic zones of the tegmentum, neuroepithelial-like cells (NECs) corresponding to cells previously described from the zebrafish cerebellum were found and characterized. In the tegmentum of juvenile chum salmon, patterns of paracrine neurosecretion were observed and their ultrastructural characteristics were recorded. Patterns of apoptosis in large neurons of the tegmentum were examined by TEM. Using immunohistochemical (IHC) labeling of the brain lipid-binding protein (BLBP) and aromatase B (AroB), patterns of their expression in the tegmentum of intact animals and in the post-traumatic period after acute injury to the medulla oblongata were characterized. The response to brainstem injury in chum salmon was found to activate multiple signaling pathways, which significantly increases the BLBP and AroB expression in various regions of the tegmentum and valvula cerebelli. However, post-traumatic patterns of BLBP and AroB localizations are not the same. In addition to a general increase in BLBP expression in the tegmental parenchyma, BLBP overexpression was observed in the rostro-lateral tegmental neurogenic zone (RLTNZ), while AroB expression in the RLTNZ was completely absent. Another difference was the peripheral overexpression of AroB and the formation of dense reactive clusters in the ventro-medial zone of the tegmentum. Thus, in the post-traumatic period, various pathways were activated whose components were putative candidates for inducers of the “astrocyte-like” response in the juvenile chum salmon brain that are similar to those present in the mammalian brain. In this case, BLBP acted as a factor enhancing the differentiation of both radial glia and neurons. Estradiol from AroB+ astrocytes exerted paracrine neuroprotective effects through the potential inhibition of inflammatory processes. These results indicate a new role for neuronal aromatization as a mechanism preventing the development of neuroinflammation. Moreover, our findings support the hypothesis that BLBP is a factor enhancing neuronal and glial differentiation in the post-traumatic period in the chum salmon brain.

In adult fish, neurogenesis occurs in many areas of the brain, including the cerebellum, with the ratio of newly formed cells relative to the total number of brain cells being several orders of magnitude greater than in mammals. Our study aimed to compare the expressions of aromatase B (AroB), glutamine synthetase (GS), and cystathionine-beta-synthase (CBS) in the cerebellum of intact juvenile chum salmon, Oncorhynchus keta. To identify the dynamics that determine the involvement of AroB, GS, and CBS in the cellular mechanisms of regeneration, we performed a comprehensive assessment of the expressions of these molecular markers during a long-term primary traumatic brain injury (TBI) and after a repeated acute TBI to the cerebellum of O. keta juveniles. As a result, in intact juveniles, weak or moderate expressions of AroB, GS, and CBS were detected in four cell types, including cells of the neuroepithelial type, migrating, and differentiated cells (graphic abstract, A). At 90 days post injury, local hypercellular areas were found in the molecular layer containing moderately labeled AroB+, GS+, and CBS+ cells of the neuroepithelial type and larger AroB+, GS+, and CBS+ cells (possibly analogous to the reactive glia of mammals); patterns of cells migration and neovascularization were also observed. A repeated TBI caused the number of AroB+, GS+, and CBS+ cells to further increase; an increased intensity of immunolabeling was recorded from all cell types (graphic abstract, C). Thus, the results of this study provide a better understanding of adult neurogenesis in teleost fishes, which is expected to clarify the issue of the reactivation of adult neurogenesis in mammalian species.