Post-hatching brain morphogenesis and cell proliferation in the pulse-type mormyrid Mormyrus rume proboscirostris

Radmilovich, Milka; Barreiro, Isabel; Iribarne, Leticia; Grant, Kirsty; Kirschbaum, Frank; Castelló, María E.

doi:10.1016/j.jphysparis.2016.11.007

Cited by 7 publications

(8 citation statements)

References 60 publications

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“…Other outstanding proliferation and migration processes occurred in the Cb of adult G. omarorum as newborn cells migrated along relatively large distances in all cerebellar divisions (CCb, VCb, and EG) as they relocate from one cerebellar layer to another. There, the migration process involved an almost complete shift of newborn cells between cerebellar layers in a period of 30 days after CldU administration, as previously shown in the Cb of this (Olivera-Pasilio, 2014 ) and other teleost species ( A. leptorhynchus : Zupanc et al, 1996 ; D rerio : Zupanc et al, 2005 ; Kaslin et al, 2009 ; C. auratus : Delgado and Schmachtenberg, 2011 ; O. mossambicus : Teles et al, 2012 ; and M. rume : Radmilovich et al, 2016 ). According to the distribution of DCX cellular process in the CCb of G. omarorum , the migration process of new born cells may involve displacements in the medial-lateral direction along the CCb-mol (as shown by Kaslin et al, 2009 ), as well as in the rostral-caudal direction in the ganglionic layer, not described previously.…”

Section: Discussionsupporting

confidence: 75%

“…The peculiar adult brain morphology of weakly electric fish is associated to the relevance of the electrosensory modality for these fish lifestyle (Evans, 1940 ; Bennett, 1971 ; Hodos and Butler, 1997 ; Kotrschal et al, 1998 ; Meek and Nieuwenhuys, 1998 ; Ito et al, 2007 ; Shumway, 2008 ). It results from the differential growth of portions of the neural tube that progressively differentiate into brain vesicles followed by the subsequent formation and differential growth of brain structures derived from the alar plate, as shown in wave (Leyhausen et al, 1987 ; Lannoo et al, 1990 ) and pulse (Iribarne and Castelló, 2014 ) gymnotids, and pulse mormyrids (Haugedé-Carré et al, 1977 , 1979 ; Radmilovich et al, 2016 ). The maintenance of adult brain morphology as fish body grows indefinitely depends in turn on heterogeneous cell proliferation and neurogenesis.…”

Section: Introductionmentioning

confidence: 99%

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Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

2017

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Adult neurogenesis, an essential mechanism of brain plasticity, enables brain development along postnatal life, constant addition of new neurons, neuronal turnover, and/or regeneration. It is amply distributed but negatively modulated during development and along evolution. Widespread cell proliferation, high neurogenic, and regenerative capacities are considered characteristics of teleost brains during adulthood. These anamniotes are promising models to depict factors that modulate cell proliferation, migration, and neurogenesis, and might be intervened to promote brain plasticity in mammals. Nevertheless, the migration path of derived cells to their final destination was not studied in various teleosts, including most weakly electric fish. In this group adult brain morphology is attributed to sensory specialization, involving the concerted evolution of peripheral electroreceptors and electric organs, encompassed by the evolution of neural networks involved in electrosensory information processing. In wave type gymnotids adult brain morphology is proposed to result from lifelong region specific cell proliferation and neurogenesis. Consistently, pulse type weakly electric gymnotids and mormyrids show widespread distribution of proliferation zones that persists in adulthood, but their neurogenic potential is still unknown. Here we studied the migration process and differentiation of newborn cells into the neuronal phenotype in the pulse type gymnotid Gymnotus omarorum. Pulse labeling of S-phase cells with 5-Chloro-2′-deoxyuridine thymidine followed by 1 to 180 day survivals evidenced long distance migration of newborn cells from the rostralmost telencephalic ventricle to the olfactory bulb, and between layers of all cerebellar divisions. Shorter migration appeared in the tectum opticum and torus semicircularis. In many brain regions, derived cells expressed early neuronal markers doublecortin (chase: 1–30 days) and HuC/HuD (chase: 7–180 days). Some newborn cells expressed the mature neuronal marker tyrosine hydroxylase in the subpallium (chase: 90 days) and olfactory bulb (chase: 180 days), indicating the acquisition of a mature neuronal phenotype. Long term CldU labeled newborn cells of the granular layer of the corpus cerebelli were also retrogradely labeled “in vivo,” suggesting their insertion into the neural networks. These findings evidence the neurogenic capacity of telencephalic, mesencephalic, and rhombencephalic brain proliferation zones in G. omarorum, supporting the phylogenetic conserved feature of adult neurogenesis and its functional significance.

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Section: Discussionsupporting

confidence: 75%

Section: Introductionmentioning

confidence: 99%

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

2017

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“…In mammals, evidence suggests that brain region scaling is tied to the order of regional neurogenesis [3]. Teleost fishes have indeterminate growth; adult neurogenesis occurs in every brain region [34,35] and is prominent in the cerebellum [35,36]. Region-specific rates of adult neurogenesis are a potential mechanism for differential growth of brain regions between species that could underlie mosaic evolution.…”

Section: Discussionmentioning

confidence: 99%

“…Region-specific rates of adult neurogenesis are a potential mechanism for differential growth of brain regions between species that could underlie mosaic evolution. A study of brain development and neurogenesis in one large-brained species of mormyrid indicated several neurogenesis zones in the cerebellum that persisted throughout life [36]. Extensive adult neurogenesis may make mosaic change more easily evolved in teleost fish than in mammals.…”

Section: Discussionmentioning

confidence: 99%

Extreme Enlargement of the Cerebellum in a Clade of Teleost Fishes that Evolved a Novel Active Sensory System

2018

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“…Testing this idea requires more knowledge of brain development in fishes. Based on the results presented in this paper, obtaining such data in Osteoglossiformes [Haugedé-Carré et al, 1977;Radmilovich et al, 2016] and linking it to data on static allometric slopes and intercepts would be particularly relevant to further advance our understanding of the mechanism of allometric constraints.…”

Section: Discussionmentioning

confidence: 99%

Exceptionally Steep Brain-Body Evolutionary Allometry Underlies the Unique Encephalization of Osteoglossiformes

Tsuboi

2021

Brain Behav Evol

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Brain-body static allometry, which is the relationship between brain size and body size within species, is thought to reflect developmental and genetic constraints. Existing evidence suggests that the evolution of large brain size without accompanying changes in body size (that is, encephalization) may occur when this constraint is relaxed. Teleost fish species are generally characterized by having close-fitting brain-body static allometries, leading to strong allometric constraints and small relative brain sizes. However, one order of teleost, Osteoglossiformes, underwent extreme encephalization, and its mechanistic bases are unknown. Here, I used a dataset and phylogeny encompassing 859 teleost species to demonstrate that the encephalization of Osteoglossiformes occurred through an increase in the slope of evolutionary (among-species) brain-body allometry. The slope is virtually isometric (1.03 ± 0.09 SE), making it one of the steepest evolutionary brain-body allometric slopes reported to date, and it deviates significantly from the evolutionary brain-body allometric slopes of other clades of teleost. Examination of the relationship between static allometric parameters (intercepts and slopes) and evolutionary allometry revealed that the dramatic steepening of the evolutionary allometric slope in Osteoglossiformes was a combined result of evolution in the slopes and intercepts of static allometry. These results suggest that the evolution of static allometry, which likely has been driven by evolutionary changes in the rate and timing of brain development, has facilitated the unique encephalization of Osteoglossiformes.

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Post-hatching brain morphogenesis and cell proliferation in the pulse-type mormyrid Mormyrus rume proboscirostris

Cited by 7 publications

References 60 publications

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

Extreme Enlargement of the Cerebellum in a Clade of Teleost Fishes that Evolved a Novel Active Sensory System

Exceptionally Steep Brain-Body Evolutionary Allometry Underlies the Unique Encephalization of Osteoglossiformes

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