Comprehensive expression map of transcription regulators in the adult zebrafish telencephalon reveals distinct neurogenic niches

Neural communication depends on release and reception of different neurotransmitters within complex circuits that ultimately mediate basic biological functions. We mapped the distribution of glutamatergic, GABAergic, and cholinergic neurons in the brain of the African cichlid fish Astatotilapia burtoni using in situ hybridization to label vesicular glutamate transporters (vglut1, vglut2.1, vglut3), glutamate decarboxylases (gad1, gad2), and choline acetyltransferase (chat). Cells expressing the glutamatergic markers vgluts 1-3 show primarily nonoverlapping distribution patterns, with the most widespread expression observed for vglut2.1, and more restricted expression of vglut1 and vglut3. vglut1 is prominent in granular layers of the cerebellum, habenula, preglomerular nuclei, and several other diencephalic, mesencephalic, and rhombencephalic regions. vglut2.1 is widely expressed in many nuclei from the olfactory bulbs to the hindbrain, while vglut3 is restricted to the hypothalamus and hindbrain. GABAergic cells show largely overlapping gad1 and gad2 expression in most brain regions. GABAergic expression dominates nuclei of the subpallial ventral telencephalon, while glutamatergic expression dominates nuclei of the pallial dorsal telencephalon. chat-expressing cells are prominent in motor cranial nerve nuclei, and some scattered cells lie in the preoptic area and ventral part of the ventral telencephalon. A localization summary of these markers within regions of the conserved social decision-making network reveals a predominance of either GABAergic or glutamatergic cells within individual nuclei. The neurotransmitter distributions described here in the brain of a single fish species provide an important resource for identification of brain nuclei in other fishes, as well as future comparative studies on circuit organization and function. J. Comp. Neurol. 525:610-638, 2017. © 2016 Wiley Periodicals, Inc.

Section: Discussionmentioning

confidence: 70%

Localization of glutamatergic, GABAergic, and cholinergic neurons in the brain of the African cichlid fish,Astatotilapia burtoni

Maruska

Butler

Field

et al. 2016

“…Type 1 and type 2 progenitors correspond to quiescent and actively dividing radial glial cells, respectively, while type 3 progenitors are believed to be actively dividing neuroblasts (März et al, ; Schmidt et al, ). Radial glial cells exhibit a wide variety of specific marker in the brain of adult zebrafish, such as Blbp (brain lipid binding protein), Gfap (glial fibrillary acidic protein), S100β (S100 calcium binding protein B), Cxcr4 (C‐X‐C chemokine receptor type 4), Id1 (inhibitor of DNA binding 1, a transcription regulator), and also the estrogen‐synthesizing enzyme, aromatase B (AroB), encoded by the cyp19a1b gene (Menuet et al, ; Tong et al, ; Diotel et al, 2015; März et al, ; Dinarello, ; Coumailleau et al, ; Rodriguez Viales et al, ). In order to investigate the presence of 5hmC in radial glial cells, we took advantage of a cyp19a1b ‐GFP transgenic fish line in which GFP is expressed in radial glial cells.…”

Section: Resultsmentioning

confidence: 99%

5‐hydroxymethylcytosine marks postmitotic neural cells in the adult and developing vertebrate central nervous system

Diotel

Mérot

Coumailleau

et al. 2016

Self Cite

The epigenetic mark 5-hydroxymethylcytosine (5hmC) is a cytosine modification that is abundant in the central nervous system of mammals and which results from 5-methylcytosine oxidation by TET enzymes. Such a mark is suggested to play key roles in the regulation of chromatin structure and gene expression. However, its precise functions still remain poorly understood and information about its distribution in non-mammalian species is still lacking. Here, the distribution of 5hmC was investigated in the brain of adult zebrafish, African claw frog, and mouse in a comparative manner. We show that zebrafish neurons are endowed with high levels of 5hmC, whereas quiescent or proliferative neural progenitors show low to undetectable levels of the modified cytosine. In the brain of larval and juvenile Xenopus, 5hmC is also detected in neurons, while ventricular proliferative cells do not display this epigenetic mark. Similarly, 5hmC is enriched in neurons compared to neural progenitors of the ventricular zone in the mouse developing cortex. Interestingly, 5hmC colocalized with the methylated DNA binding protein MeCP2 and with the active chromatin histone modification H3K4me2 in mouse neurons. Taken together, our results show an evolutionarily conserved cerebral distribution of 5hmC between fish and tetrapods and reinforce the idea that 5hmC fulfills major functions in the control of chromatin activity in vertebrate neurons. J. Comp. Neurol. 525:478-497, 2017. © 2016 Wiley Periodicals, Inc.

“…However, here we show newly a shh‐ GFP expressing population in the adult zebrafish pallial telencephalon, that is, pallial radial glia cells. Various studies have shown that mitotic stem cells (radial glia) exist in the adult zebrafish telencephalon along the subpallial and pallial ventricular lining (e.g., Chapouton, Jagasia, & Bally‐Cuif, ; Diotel et al, ; Kaslin, Ganz, & Brand, ; Lillesaar, Stigloher, Tannhäuser, Wullimann, & Bally‐Cuif, ; Lindsey, Darabie, & Tropepe, ; März, Schmidt, Rastegar, & Strähle, ; Than‐Trong & Bally‐Cuif, ). However, to the best of our knowledge, a role for shh has not been shown in adult telencephalic stem cells.…”

Section: Discussionmentioning

confidence: 99%

Sonic hedgehog expression in zebrafish forebrain identifies the teleostean pallidal signaling center and shows preglomerular complex and posterior tubercular dopamine cells to arise from shh cells

Wullimann

Umeasalugo

2019

Ventralization, a major patterning process in the developing vertebrate neural tube (central nervous system, CNS), depends on Sonic hedgehog (SHH) as a main signaling morphogen. We studied the CNS of late larval and young adult zebrafish in a transgenic shh‐GFP line revealing increased neuroanatomical detail due to the progressed differentiation state compared to earlier stages. Some major findings emerge from the present study. (a) shh –GFP is still expressed along the adult zebrafish CNS neuraxis in most locations seen in larvae. (b) We newly identify a ventroposterior shh pallidal domain representing the basal telencephalic signaling center important for basal ganglia development known in other vertebrates (i.e., the anterior entopeduncular area—basal medial ganglionic eminence of mammals). (c) We further show late‐emerging shh‐GFP positive radial glia cells in the medial zone of the dorsal telencephalon (i.e., the teleostan pallial amygdala). (d) Immunostains for tyrosine hydroxylase demonstrate that there is selective colocalization in adult dopamine cells with shh‐GFP in the posterior tuberculum, including in projection cells to striatum, which represents a striking parallel to amniote mesodiencephalic dopamine cell origin from shh expressing floor plate cells. (e) There is no colocalization of shh and islet1 as shown by respective shh‐GFP and islet1‐GFP lines. (f) The only radially far migrated shh‐GFP cells are located in the preglomerular area. (g) There are no adult cerebellar and tectal shh‐GFP cells confirming their exclusive role during early development as previously reported by our laboratory.