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

View Article: PubMed Central - PubMed

ABSTRACT

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.

No MeSH data available.


Regionalization of the alar hypothalamus and neighbor territories in embryos of Scyliorhinus canicula at stages 29–31 based on the expression of ScOtp(A–D) and ScDlx2/5(E–J) expression by means of single in situ hybridization (ISH) (A–J) and/or combined with immunohistochemistry (J) on sagittal (A,D,E,H–J) or transverse (B,C,F,G) sections. Continuous red line: ABB. Dashed red line: IHB. Gray line: HTB. Continuous black line divides dorso-ventral division of the alar hypothalamus into Pa (dorsal) and SPa (ventral) territories. Dashed black line represents subdivisions inside the SPa into SPa dorsal (SPaD) and ventral (SPaV). Asterisk point the PThE (ap3). (A–D)ScOtp expression in the Pa at indicated stages. ScOtp labeling (yellow arrowheads) in the SPa corresponds to marginal cells. Black arrowheads point to ScOtp-expressing cells in the subpallium. Red arrowheads point to ScOtp-expressing cells in the pallium. Blue arrowheads point to marginal ScOtp-expressing cells in the Pa. Yellow arrowheads point to ScOtp-expressing cells ventral to the Pa. (A′) Detail of a region equivalent to that squared area in (A) to show ScOtp-expressing cells ventral to the Pa rostrally. (E–J)ScDlx2/5 expression in the subpallium, SPa and ap3 at indicated stages. Red arrowhead points to the lack of expression in the pallium. White arrowheads point to ScDlx2-expressing (F′) cells in the marginal zone of the Pa. Green arrowhead in (G) points to ScDlx2/5 expression in the RTu. (J) Detail of a region equivalent to that squared in (I). Arrows point to 5-HT-ir tracts coursing in the marginal Pa and SPa. For abbreviations, see list.
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Figure 1: Regionalization of the alar hypothalamus and neighbor territories in embryos of Scyliorhinus canicula at stages 29–31 based on the expression of ScOtp(A–D) and ScDlx2/5(E–J) expression by means of single in situ hybridization (ISH) (A–J) and/or combined with immunohistochemistry (J) on sagittal (A,D,E,H–J) or transverse (B,C,F,G) sections. Continuous red line: ABB. Dashed red line: IHB. Gray line: HTB. Continuous black line divides dorso-ventral division of the alar hypothalamus into Pa (dorsal) and SPa (ventral) territories. Dashed black line represents subdivisions inside the SPa into SPa dorsal (SPaD) and ventral (SPaV). Asterisk point the PThE (ap3). (A–D)ScOtp expression in the Pa at indicated stages. ScOtp labeling (yellow arrowheads) in the SPa corresponds to marginal cells. Black arrowheads point to ScOtp-expressing cells in the subpallium. Red arrowheads point to ScOtp-expressing cells in the pallium. Blue arrowheads point to marginal ScOtp-expressing cells in the Pa. Yellow arrowheads point to ScOtp-expressing cells ventral to the Pa. (A′) Detail of a region equivalent to that squared area in (A) to show ScOtp-expressing cells ventral to the Pa rostrally. (E–J)ScDlx2/5 expression in the subpallium, SPa and ap3 at indicated stages. Red arrowhead points to the lack of expression in the pallium. White arrowheads point to ScDlx2-expressing (F′) cells in the marginal zone of the Pa. Green arrowhead in (G) points to ScDlx2/5 expression in the RTu. (J) Detail of a region equivalent to that squared in (I). Arrows point to 5-HT-ir tracts coursing in the marginal Pa and SPa. For abbreviations, see list.

Mentions: At stage 29, ScOtp is expressed in the surroundings of the optic stalk and caudally beyond, in what mainly represents the Pa histogenetic domain, as seen in sagittal (Figure 1A) and transverse (Figures 1B,C) sections. ScOtp is recognized in individual cells in the TPa domain (Figure 1B) mostly located in the marginal zone (blue arrowhead in Figure 1B) but also scattered through the ventricular zone. Similarly, in the PPa domain (Figure 1C), ScOtp is mainly expressed in the marginal zone (blue arrowheads in Figure 1C), while scarce ScOtp-expressing cells are observed in the ventricular zone. Furthermore, ScOtp-expressing cells are recognized in the marginal zone of territories placed dorsal and ventral with respect to the TPa/PPa domain, forming a continuous stream with the marginal ScOtp-expressing cells of this domain. Particularly noticeable are the strings of ScOtp-expressing cells dorsally extended from the TPa domain into the subpallial territory (black arrowheads in Figures 1A,B) and from the rostral-most portion of the PPa domain into the pallium (red arrowheads in Figures 1A,C). ScOtp-expressing cells are also observed in the marginal zone ventral to the TPa/PPa domain. These cells cannot be observed at the rostral-most TSPa domain (Figure 1B) but they spread just caudal from this point into the remaining TSPa/PSPa domain (yellow arrowheads in Figures 1A′,C). Of note, these ventral ScOtp-expressing cells are distributed into the dorsal-most marginal zone of TSPa/PSPa domains (yellow arrowhead in Figure 1C) but they spread through the SPa domain by late stage 29 (not shown).


The Shark Alar Hypothalamus: Molecular Characterization of Prosomeric Subdivisions and Evolutionary Trends
Regionalization of the alar hypothalamus and neighbor territories in embryos of Scyliorhinus canicula at stages 29–31 based on the expression of ScOtp(A–D) and ScDlx2/5(E–J) expression by means of single in situ hybridization (ISH) (A–J) and/or combined with immunohistochemistry (J) on sagittal (A,D,E,H–J) or transverse (B,C,F,G) sections. Continuous red line: ABB. Dashed red line: IHB. Gray line: HTB. Continuous black line divides dorso-ventral division of the alar hypothalamus into Pa (dorsal) and SPa (ventral) territories. Dashed black line represents subdivisions inside the SPa into SPa dorsal (SPaD) and ventral (SPaV). Asterisk point the PThE (ap3). (A–D)ScOtp expression in the Pa at indicated stages. ScOtp labeling (yellow arrowheads) in the SPa corresponds to marginal cells. Black arrowheads point to ScOtp-expressing cells in the subpallium. Red arrowheads point to ScOtp-expressing cells in the pallium. Blue arrowheads point to marginal ScOtp-expressing cells in the Pa. Yellow arrowheads point to ScOtp-expressing cells ventral to the Pa. (A′) Detail of a region equivalent to that squared area in (A) to show ScOtp-expressing cells ventral to the Pa rostrally. (E–J)ScDlx2/5 expression in the subpallium, SPa and ap3 at indicated stages. Red arrowhead points to the lack of expression in the pallium. White arrowheads point to ScDlx2-expressing (F′) cells in the marginal zone of the Pa. Green arrowhead in (G) points to ScDlx2/5 expression in the RTu. (J) Detail of a region equivalent to that squared in (I). Arrows point to 5-HT-ir tracts coursing in the marginal Pa and SPa. For abbreviations, see list.
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Figure 1: Regionalization of the alar hypothalamus and neighbor territories in embryos of Scyliorhinus canicula at stages 29–31 based on the expression of ScOtp(A–D) and ScDlx2/5(E–J) expression by means of single in situ hybridization (ISH) (A–J) and/or combined with immunohistochemistry (J) on sagittal (A,D,E,H–J) or transverse (B,C,F,G) sections. Continuous red line: ABB. Dashed red line: IHB. Gray line: HTB. Continuous black line divides dorso-ventral division of the alar hypothalamus into Pa (dorsal) and SPa (ventral) territories. Dashed black line represents subdivisions inside the SPa into SPa dorsal (SPaD) and ventral (SPaV). Asterisk point the PThE (ap3). (A–D)ScOtp expression in the Pa at indicated stages. ScOtp labeling (yellow arrowheads) in the SPa corresponds to marginal cells. Black arrowheads point to ScOtp-expressing cells in the subpallium. Red arrowheads point to ScOtp-expressing cells in the pallium. Blue arrowheads point to marginal ScOtp-expressing cells in the Pa. Yellow arrowheads point to ScOtp-expressing cells ventral to the Pa. (A′) Detail of a region equivalent to that squared area in (A) to show ScOtp-expressing cells ventral to the Pa rostrally. (E–J)ScDlx2/5 expression in the subpallium, SPa and ap3 at indicated stages. Red arrowhead points to the lack of expression in the pallium. White arrowheads point to ScDlx2-expressing (F′) cells in the marginal zone of the Pa. Green arrowhead in (G) points to ScDlx2/5 expression in the RTu. (J) Detail of a region equivalent to that squared in (I). Arrows point to 5-HT-ir tracts coursing in the marginal Pa and SPa. For abbreviations, see list.
Mentions: At stage 29, ScOtp is expressed in the surroundings of the optic stalk and caudally beyond, in what mainly represents the Pa histogenetic domain, as seen in sagittal (Figure 1A) and transverse (Figures 1B,C) sections. ScOtp is recognized in individual cells in the TPa domain (Figure 1B) mostly located in the marginal zone (blue arrowhead in Figure 1B) but also scattered through the ventricular zone. Similarly, in the PPa domain (Figure 1C), ScOtp is mainly expressed in the marginal zone (blue arrowheads in Figure 1C), while scarce ScOtp-expressing cells are observed in the ventricular zone. Furthermore, ScOtp-expressing cells are recognized in the marginal zone of territories placed dorsal and ventral with respect to the TPa/PPa domain, forming a continuous stream with the marginal ScOtp-expressing cells of this domain. Particularly noticeable are the strings of ScOtp-expressing cells dorsally extended from the TPa domain into the subpallial territory (black arrowheads in Figures 1A,B) and from the rostral-most portion of the PPa domain into the pallium (red arrowheads in Figures 1A,C). ScOtp-expressing cells are also observed in the marginal zone ventral to the TPa/PPa domain. These cells cannot be observed at the rostral-most TSPa domain (Figure 1B) but they spread just caudal from this point into the remaining TSPa/PSPa domain (yellow arrowheads in Figures 1A′,C). Of note, these ventral ScOtp-expressing cells are distributed into the dorsal-most marginal zone of TSPa/PSPa domains (yellow arrowhead in Figure 1C) but they spread through the SPa domain by late stage 29 (not shown).

View Article: PubMed Central - PubMed

ABSTRACT

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.

No MeSH data available.