Identification of the optic recess region as a morphogenetic entity in the zebrafish forebrain

Affaticati, Pierre; Yamamoto, Kei; Rizzi, B; Bureau, Charlotte; Peyriéras, Nadine; Pasqualini, Catherine; Demarque, Michaël; Vernier, Philippe

doi:10.1038/srep08738

Cited by 57 publications

(87 citation statements)

References 68 publications

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“…Firstly, although the abutted expression of Foxg1 / Otp is assumed to define the HTB, Foxg1 has also been described beyond the telencephalic stalk (Pratt et al, 2004; Affaticati et al, 2015; Santos-Durán et al, 2015) questioning its telencephalon-restricted identity and thus the existence of the HTB at this place. Besides, in Foxg1 null mutant mice the ventral, but not the dorsal, telencephalon is lost (Xuan et al, 1995; Martynoga et al, 2005), which suggests it is required for the development of the subpallium but maybe not for the whole telencephalon.…”

Section: Discussionmentioning

confidence: 99%

“…Noteworthy, recently Affaticati et al (2015) propose the orr (optic recess region) as a morphogenetic entity including Dlx2 subdomains dorsal and ventral to Otp expression in the alar hypothalamus. These Dlx -expresing subdomains likely co-distribute with Pax6 as has been described in the pallium-subpallium boundary (Flames et al, 2007; Ferreiro-Galve et al, 2008) and in the SPaD (present results) pointing to Pax6 as an important factor patterning the alar and rostral-most prosencephalon.…”

Section: Discussionmentioning

confidence: 99%

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The Shark Alar Hypothalamus: Molecular Characterization of Prosomeric Subdivisions and Evolutionary Trends

Santos-Durán¹,

Ferreiro-Galve²,

Menuet³

et al. 2016

Front. Neuroanat.

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The hypothalamus is an important physiologic center of the vertebrate brain involved in the elaboration of individual and species survival responses. To better understand the ancestral organization of the alar hypothalamus we revisit previous data on ScOtp, ScDlx2/5, ScTbr1, ScNkx2.1 expression and Pax6 immunoreactivity jointly with new data on ScNeurog2, ScLhx9, ScLhx5, and ScNkx2.8 expression, in addition to immunoreactivity to serotonin (5-HT) and doublecortin (DCX) in the catshark Scyliorhinus canicula, a key species for this purpose since cartilaginous fishes are basal representatives of gnathostomes (jawed vertebrates). Our study revealed a complex genoarchitecture for the chondrichthyan alar hypothalamus. We identified terminal (rostral) and peduncular (caudal) subdivisions in the prosomeric paraventricular and subparaventricular areas (TPa/PPa and TSPa/PSPa, respectively) evidenced by the expression pattern of developmental genes like ScLhx5 (TPa) and immunoreactivity against Pax6 (PSPa) and 5-HT (PPa and PSPa). Dorso-ventral subdivisions were only evidenced in the SPa (SPaD, SPaV; respectively) by means of Pax6 and ScNkx2.8 (respectively). Interestingly, ScNkx2.8 expression overlaps over the alar-basal boundary, as Nkx2.2 does in other vertebrates. Our results reveal evidences for the existence of different groups of tangentially migrated cells expressing ScOtp, Pax6, and ScDlx2. The genoarchitectonic comparative analysis suggests alternative interpretations of the rostral-most alar plate in prosomeric terms and reveals a conserved molecular background for the vertebrate alar hypothalamus likely acquired before/during the agnathan-gnathostome transition, on which Otp, Pax6, Lhx5, and Neurog2 are expressed in the Pa while Dlx and Nkx2.2/Nkx2.8 are expressed in the SPa.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The Shark Alar Hypothalamus: Molecular Characterization of Prosomeric Subdivisions and Evolutionary Trends

Santos-Durán¹,

Ferreiro-Galve²,

Menuet³

et al. 2016

Front. Neuroanat.

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“…The new model of the forebrain regionalization also clarifies the homology of the Otp ‐dependent neuroendocrine cell population (Affaticati et al . ). In both amniotes and teleosts, several categories of neuroendocrine cells regulating pituitary functions are located in the territory expressing the transcription factor Otp .…”

Section: Optic Recess Region (Orr): a Morphogenetic Unit Organized Armentioning

confidence: 97%

“…(C) A new model proposed by Affaticati et al . (), in which the secondary prosencephalon is divided into three parts, the telencephalon, hypothalamus, and optic recess region ( ORR ). At the bottom, 3D illustration (left; modified from Picker et al .…”

Section: Different Models Of Forebrain Regionalization: Columnar Versmentioning

confidence: 99%

New perspective on the regionalization of the anterior forebrain in Osteichthyes

2017

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In the current model, the most anterior part of the forebrain (secondary prosencephalon) is subdivided into the telencephalon dorsally and the hypothalamus ventrally. Our recent study identified a new morphogenetic unit named the optic recess region (ORR) between the telencephalon and the hypothalamus. This modification of the forebrain regionalization based on the ventricular organization resolved some previously unexplained inconsistency about regional identification in different vertebrate groups. The ventricular-based comparison also revealed a large diversity within the subregions (notably in the hypothalamus and telencephalon) among different vertebrate groups. In tetrapods there is only one hypothalamic recess, while in teleosts there are two recesses. Most notably, the mammalian and teleost hypothalami are two extreme cases: the former has lost the cerebrospinal fluid-contacting (CSF-c) neurons, while the latter has increased them. Thus, one to one homology of hypothalamic subregions in mammals and teleosts requires careful verification. In the telencephalon, different developmental processes between Sarcopterygii (lobe-finned fish) and Actinopterygii (ray-finned fish) have already been described: the evagination and the eversion. Although pallial homology has been long discussed based on the assumption that the medial-lateral organization of the pallium in Actinopterygii is inverted from that in Sarcopterygii, recent developmental data contradict this assumption. Current models of the brain organization are largely based on a mammalian-centric point of view, but our comparative analyses shed new light on the brain organization of Osteichthyes.

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“…Since the CSF‐c cells are located along the ventricular wall, their organization largely depends on the configuration of the hypothalamic recess. We thus took into account the ventricular morphology in our analysis, as we recently did to study the regionalization of the optic recess region (ORR) (Affaticati et al, ).…”

Section: Introductionmentioning

confidence: 99%

Comparative analysis of monoaminergic cerebrospinal fluid‐contacting cells in Osteichthyes (bony vertebrates)

Xavier

Fontaine

Bloch

et al. 2017

J of Comparative Neurology

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Cerebrospinal fluid-contacting (CSF-c) cells containing monoamines such as dopamine (DA) and serotonin (5-HT) occur in the periventricular zones of the hypothalamic region of most vertebrates except for placental mammals. Here we compare the organization of the CSF-c cells in chicken, Xenopus, and zebrafish, by analyzing the expression of synthetic enzymes of DA and 5-HT, respectively, tyrosine hydroxylase (TH) and tryptophan hydroxylase (TPH), and draw an evolutionary scenario for this cell population. Due to the lack of TH immunoreactivity in this region, the hypothalamic CSF-c cells have been thought to take up DA from the ventricle instead of synthesizing it. We demonstrate that a second TH gene (TH2) is expressed in the CSF-c cells of all the three species, suggesting that these cells do indeed synthetize DA. Furthermore, we found that many CSF-c cells coexpress TH2 and TPH1 and contain both DA and 5-HT, a dual neurotransmitter phenotype hitherto undescribed in the brain of any vertebrate. The similarities of CSF-c cells in chicken, Xenopus, and zebrafish suggest that these characteristics are inherited from the common ancestor of the Osteichthyes. A significant difference between tetrapods and teleosts is that teleosts possess an additional CSF-c cell population around the posterior recess (PR) that has emerged in specific groups of Actinopterygii. Our comparative analysis reveals that the hypothalamus in mammals and teleosts has evolved in a divergent manner: placental mammals have lost the monoaminergic CSF-c cells, while teleosts have increased their relative number. K E Y W O R D S

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Identification of the optic recess region as a morphogenetic entity in the zebrafish forebrain

Cited by 57 publications

References 68 publications

The Shark Alar Hypothalamus: Molecular Characterization of Prosomeric Subdivisions and Evolutionary Trends

The Shark Alar Hypothalamus: Molecular Characterization of Prosomeric Subdivisions and Evolutionary Trends

New perspective on the regionalization of the anterior forebrain in Osteichthyes

Comparative analysis of monoaminergic cerebrospinal fluid‐contacting cells in Osteichthyes (bony vertebrates)

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