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Prosomeric organization of the hypothalamus in an elasmobranch, the catshark Scyliorhinus canicula.

Santos-Durán GN, Menuet A, Lagadec R, Mayeur H, Ferreiro-Galve S, Mazan S, Rodríguez-Moldes I, Candal E - Front Neuroanat (2015)

Bottom Line: Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain.Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates.These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

View Article: PubMed Central - PubMed

Affiliation: Centro de Investigaciones Biológicas, Department of Cell Biology and Ecology, University of Santiago de Compostela Santiago de Compostela, Spain.

ABSTRACT
The hypothalamus has been a central topic in neuroanatomy because of its important physiological functions, but its mature organization remains elusive. Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain. Here we studied the molecular organization of the hypothalamus and neighboring telencephalic domains in a cartilaginous fish, the catshark, Scyliorhinus canicula, focusing on ScFoxg1a, ScShh, ScNkx2.1, ScDlx2/5, ScOtp, and ScTbr1 expression profiles and on the identification α-acetylated-tubulin-immunoreactive (ir), TH-ir, 5-HT-ir, and GFAP-ir structures by means of immunohistochemistry. Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates. These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

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Regionalization of the shark hypothalamus from stages 29–31 based on immunoreactivity to Shh (A,B,B′,D,I–N), TH (B′), 5-HT (I–L), GFAP (O, P) and expression of ScNkx2.1 (C,C′,D,G″), ScDlx2/5(E,E′,F,M) and ScOtp(G,G′, G″, H, H′, N) genes by means of single immunohistochemistry (IHC; A,B,O,P), double IHC (B′,I–L), single ISH (C,E,E′,F,G, G′,H,H′) and/or combined with IHC (D,M,N) on sagittal (A,B,B′,C–G,G″,H–J,M,N) or transverse sections (C′,E′,G′,H′,K,L,O,P). Image in (G″) results from the overlapping of two parallel sections respectively hybridized with ScOtp and ScNkx2.1 probes. Color for ScNkx2.1 was digitally converted to brown to ease comparison. Dotted lines define the hypothalamo-telencephalic boundary (HTB), dashed lines indicate the caudal border of the secondary prosencephalon, red lines indicate the ABB and continuous black lines represent the path followed by 5-HT-ir fibers. (A) Shh-immunoreactivity was observed in the most caudo-ventral part of the CBHy (arrow) and in the RBHy. The arrowhead points to the zli. (B) Shh-immunoreactivity was observed in the telencephalon (arrowhead) beyond the territory of the anterior commissure (asterisk). The arrow points to Shh-immunoreactivity in the caudal-most CBHy. (B′) Detail of the squared area in (B) to show Shh- and TH-immunoreactivity in its most caudo-ventral part (arrow). (C,D)ScNkx2.1 expression was observed in the hypothalamus and telencephalon. A detail of a transverse section at the level indicated in (C) is shown in (C′). The arrows in (C,C′,D) point to ScNkx2.1-expressing cells in the mantle zone of the most caudo-ventral CBHy. The arrowheads in (C,D) indicate a wedge-shaped domain lacking ScNkx2.1 expression. The asterisk in (D) indicates the territory of the anterior commissure. (E,F)ScDlx2/5 expression was observed in p3 and in the secondary prosencephalon. A detail of a transverse section at the level indicated in (D) is shown in (D′). The arrow in (E,E′) points to ScDlx2/5-expressing cells in the mantle of the p3Tg. The star in (E,E′) indicates the prospective territory of the PThE. The black asterisks in (E,F) indicate a gap of ScDlx2/5 expression in the telencephalon. The arrowheads in (E,F) point to ScDlx2/5 expression in the BHy. (G,H)ScOtp expression in the hypothalamus. Details in (G′,H′) correspond to transverse sections at the levels indicated in (G,H). Detail in (G″) correspond to the squared area in (G). The arrows in (G,G″) point to the ventricular domain expressing ScOtp in the caudal CBHy. The black arrowheads in (G,G″, H′) point to ScOtp-expressing cells in the mantle of the most caudo-ventral part of CBHy and p3Tg. The arrow in (G″) indicates a domain expressing ScNkx2.1 alone. The white asterisks in (G′,H) indicate ScOtp-expressing cells in the mantle zone. The black arrowhead in (H) points to ScOtp-expressing cells in the AHy and the white arrowhead in (H) points to ScOtp-expressing cells between the alar and basal domains. (I–L) Double Shh- and 5-HT-immunoreactivity. (K,L) correspond to trasverse sections at the level indicated in (J). 5-HT-ir fibers in (I) are observed in the basal plate of the secondary prosencephalon. In the rostral hypothalamus such fibers coursed among RAHy and RBHy, and were located dorsally to Shh-immunoreactivity (I,J). Note the presence of 5-HT-ir fibers in the Sp (I,J,L). The white arrowhead in (J,K) points to 5-HT-ir fibers that course in the rostral CAHy. The black arrowhead in (J,L) points to 5-HT-ir fibers in the telencephalon. The arrow in (J,K) points to 5-HT-ir fibers decussating in the CBHy. The arrow in (L) points to the faint Shh immunoreactivity in the zli. (M,N) Shh IHC combined with ScDlx2/5 expression (M) or ScOtp expression (N). A gap of expression is observed between the rostral and caudal domains of ScDlx2/5 and ScOtp expression, which appeared to coincide with the path followed by 5-HT-ir fibers. (O) GFAP-ir processes at the level shown in (J). The arrowhead points to the GFAP-ir processes among RAHy and Sp. The arrow points to the GFAP-ir processes in the CBHy. (P) GFAP-ir processes at the level shown in (J). The arrow points to GFAP-ir processes in the Sp. For abbreviations, see list.
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Figure 4: Regionalization of the shark hypothalamus from stages 29–31 based on immunoreactivity to Shh (A,B,B′,D,I–N), TH (B′), 5-HT (I–L), GFAP (O, P) and expression of ScNkx2.1 (C,C′,D,G″), ScDlx2/5(E,E′,F,M) and ScOtp(G,G′, G″, H, H′, N) genes by means of single immunohistochemistry (IHC; A,B,O,P), double IHC (B′,I–L), single ISH (C,E,E′,F,G, G′,H,H′) and/or combined with IHC (D,M,N) on sagittal (A,B,B′,C–G,G″,H–J,M,N) or transverse sections (C′,E′,G′,H′,K,L,O,P). Image in (G″) results from the overlapping of two parallel sections respectively hybridized with ScOtp and ScNkx2.1 probes. Color for ScNkx2.1 was digitally converted to brown to ease comparison. Dotted lines define the hypothalamo-telencephalic boundary (HTB), dashed lines indicate the caudal border of the secondary prosencephalon, red lines indicate the ABB and continuous black lines represent the path followed by 5-HT-ir fibers. (A) Shh-immunoreactivity was observed in the most caudo-ventral part of the CBHy (arrow) and in the RBHy. The arrowhead points to the zli. (B) Shh-immunoreactivity was observed in the telencephalon (arrowhead) beyond the territory of the anterior commissure (asterisk). The arrow points to Shh-immunoreactivity in the caudal-most CBHy. (B′) Detail of the squared area in (B) to show Shh- and TH-immunoreactivity in its most caudo-ventral part (arrow). (C,D)ScNkx2.1 expression was observed in the hypothalamus and telencephalon. A detail of a transverse section at the level indicated in (C) is shown in (C′). The arrows in (C,C′,D) point to ScNkx2.1-expressing cells in the mantle zone of the most caudo-ventral CBHy. The arrowheads in (C,D) indicate a wedge-shaped domain lacking ScNkx2.1 expression. The asterisk in (D) indicates the territory of the anterior commissure. (E,F)ScDlx2/5 expression was observed in p3 and in the secondary prosencephalon. A detail of a transverse section at the level indicated in (D) is shown in (D′). The arrow in (E,E′) points to ScDlx2/5-expressing cells in the mantle of the p3Tg. The star in (E,E′) indicates the prospective territory of the PThE. The black asterisks in (E,F) indicate a gap of ScDlx2/5 expression in the telencephalon. The arrowheads in (E,F) point to ScDlx2/5 expression in the BHy. (G,H)ScOtp expression in the hypothalamus. Details in (G′,H′) correspond to transverse sections at the levels indicated in (G,H). Detail in (G″) correspond to the squared area in (G). The arrows in (G,G″) point to the ventricular domain expressing ScOtp in the caudal CBHy. The black arrowheads in (G,G″, H′) point to ScOtp-expressing cells in the mantle of the most caudo-ventral part of CBHy and p3Tg. The arrow in (G″) indicates a domain expressing ScNkx2.1 alone. The white asterisks in (G′,H) indicate ScOtp-expressing cells in the mantle zone. The black arrowhead in (H) points to ScOtp-expressing cells in the AHy and the white arrowhead in (H) points to ScOtp-expressing cells between the alar and basal domains. (I–L) Double Shh- and 5-HT-immunoreactivity. (K,L) correspond to trasverse sections at the level indicated in (J). 5-HT-ir fibers in (I) are observed in the basal plate of the secondary prosencephalon. In the rostral hypothalamus such fibers coursed among RAHy and RBHy, and were located dorsally to Shh-immunoreactivity (I,J). Note the presence of 5-HT-ir fibers in the Sp (I,J,L). The white arrowhead in (J,K) points to 5-HT-ir fibers that course in the rostral CAHy. The black arrowhead in (J,L) points to 5-HT-ir fibers in the telencephalon. The arrow in (J,K) points to 5-HT-ir fibers decussating in the CBHy. The arrow in (L) points to the faint Shh immunoreactivity in the zli. (M,N) Shh IHC combined with ScDlx2/5 expression (M) or ScOtp expression (N). A gap of expression is observed between the rostral and caudal domains of ScDlx2/5 and ScOtp expression, which appeared to coincide with the path followed by 5-HT-ir fibers. (O) GFAP-ir processes at the level shown in (J). The arrowhead points to the GFAP-ir processes among RAHy and Sp. The arrow points to the GFAP-ir processes in the CBHy. (P) GFAP-ir processes at the level shown in (J). The arrow points to GFAP-ir processes in the Sp. For abbreviations, see list.

Mentions: ScShh expression was detected during gastrulation (stage 12) in the caudal midline of the embryo (data not shown). At stage 14, during early neurulation, it has been detected in the axial mesoderm of the notochord and the prechordal plate and in the ectoderm of the caudal midline (data not shown). After the closure of the neural tube (stage 17), the signal was detected as a ventral longitudinal continuous band that extends from the caudal end of the spinal cord to the At of the forebrain, roughly at the level of the optic stalk (Figure 3D). As in other vertebrates (Shimamura et al., 1995), the expression of ScShh can be used to define the alar-basal boundary (ABB; Figures 3E–H). At stage 19, ScShh expression became downregulated in the forebrain to progressively give rise to a caudal and a rostral domain (arrow in Figures 3E–H). The narrow transverse and dorsally directed stripe of ScShh-expressing cells within the caudal domain was identified as the developing zona limitans intrathalamica (zli; arrowhead in Figure 3G). The rostral border of the ScShh caudal domain, in turn, was somewhat extended rostral to the HDB (Puelles et al., 2012), which at this stage was identified as the point where the neural tube expands to acquire the distinctive shape of the ventral hypothalamus. Therefore, the BHy appeared to be divided in three domains: two positive for ScShh (one rostral and other caudal) and one (intermediate) negative for ScShh (arrow in Figures 3G,H; see also Figure 5H in Compagnucci et al., 2013). Of note, the dorsal border of the rostral domain (presumably corresponding to the ABB) seems to codistribute with α-acetylated-tubulin-immunoreactive (-ir) longitudinal tracts (arrowheads in Figure 3I). At stage 24 (Figure 3H), a new domain emerged within the telencephalon. This short domain (arrowhead in Figure 3H) extended from a region located dorsally to the optic stalk without reaching the prospective territory of the anterior commissure (that can be identified at early development by means of α-tubulin-immunoreactivity; asterisk in Figures 3H,I). A clear gap of expression was observed between this telencephalic domain and the rostral hypothalamic one (Figure 3H). The telencephalic domain was located medially while the hypothalamic one also expanded laterally (not shown). From stage 27 onward the zli expanded dorsally toward the roof plate (arrowhead in Figure 4A). At stage 29 the medio-lateral histologic organization of the developing walls of the forebrain become more evident. As in previous developmental stages, Shh immunoreactivity was clearly identified in the basal plate of the diencephalon entering the caudo-ventral part of the BHy (arrow in Figures 4A,B,B′) and in the rostro-dorsal part of the BHy (Figures 4A,B), so that a clear negative gap of Shh-immunoreactivity occupied most of the caudal BHy (CBHy; Figures 4A,B) and part of the rostral BHy (RBHy). In the telencephalon, Shh-immunoreactivity expanded caudally beyond the prospective territory of the anterior commissure (arrowhead in Figure 4B; compare with Figure 3H). Of note, from late stage 30 onward, Shh-immunoreactivity is downregulated in the CBHy and basal diencephalon, except in the zli (data not shown).


Prosomeric organization of the hypothalamus in an elasmobranch, the catshark Scyliorhinus canicula.

Santos-Durán GN, Menuet A, Lagadec R, Mayeur H, Ferreiro-Galve S, Mazan S, Rodríguez-Moldes I, Candal E - Front Neuroanat (2015)

Regionalization of the shark hypothalamus from stages 29–31 based on immunoreactivity to Shh (A,B,B′,D,I–N), TH (B′), 5-HT (I–L), GFAP (O, P) and expression of ScNkx2.1 (C,C′,D,G″), ScDlx2/5(E,E′,F,M) and ScOtp(G,G′, G″, H, H′, N) genes by means of single immunohistochemistry (IHC; A,B,O,P), double IHC (B′,I–L), single ISH (C,E,E′,F,G, G′,H,H′) and/or combined with IHC (D,M,N) on sagittal (A,B,B′,C–G,G″,H–J,M,N) or transverse sections (C′,E′,G′,H′,K,L,O,P). Image in (G″) results from the overlapping of two parallel sections respectively hybridized with ScOtp and ScNkx2.1 probes. Color for ScNkx2.1 was digitally converted to brown to ease comparison. Dotted lines define the hypothalamo-telencephalic boundary (HTB), dashed lines indicate the caudal border of the secondary prosencephalon, red lines indicate the ABB and continuous black lines represent the path followed by 5-HT-ir fibers. (A) Shh-immunoreactivity was observed in the most caudo-ventral part of the CBHy (arrow) and in the RBHy. The arrowhead points to the zli. (B) Shh-immunoreactivity was observed in the telencephalon (arrowhead) beyond the territory of the anterior commissure (asterisk). The arrow points to Shh-immunoreactivity in the caudal-most CBHy. (B′) Detail of the squared area in (B) to show Shh- and TH-immunoreactivity in its most caudo-ventral part (arrow). (C,D)ScNkx2.1 expression was observed in the hypothalamus and telencephalon. A detail of a transverse section at the level indicated in (C) is shown in (C′). The arrows in (C,C′,D) point to ScNkx2.1-expressing cells in the mantle zone of the most caudo-ventral CBHy. The arrowheads in (C,D) indicate a wedge-shaped domain lacking ScNkx2.1 expression. The asterisk in (D) indicates the territory of the anterior commissure. (E,F)ScDlx2/5 expression was observed in p3 and in the secondary prosencephalon. A detail of a transverse section at the level indicated in (D) is shown in (D′). The arrow in (E,E′) points to ScDlx2/5-expressing cells in the mantle of the p3Tg. The star in (E,E′) indicates the prospective territory of the PThE. The black asterisks in (E,F) indicate a gap of ScDlx2/5 expression in the telencephalon. The arrowheads in (E,F) point to ScDlx2/5 expression in the BHy. (G,H)ScOtp expression in the hypothalamus. Details in (G′,H′) correspond to transverse sections at the levels indicated in (G,H). Detail in (G″) correspond to the squared area in (G). The arrows in (G,G″) point to the ventricular domain expressing ScOtp in the caudal CBHy. The black arrowheads in (G,G″, H′) point to ScOtp-expressing cells in the mantle of the most caudo-ventral part of CBHy and p3Tg. The arrow in (G″) indicates a domain expressing ScNkx2.1 alone. The white asterisks in (G′,H) indicate ScOtp-expressing cells in the mantle zone. The black arrowhead in (H) points to ScOtp-expressing cells in the AHy and the white arrowhead in (H) points to ScOtp-expressing cells between the alar and basal domains. (I–L) Double Shh- and 5-HT-immunoreactivity. (K,L) correspond to trasverse sections at the level indicated in (J). 5-HT-ir fibers in (I) are observed in the basal plate of the secondary prosencephalon. In the rostral hypothalamus such fibers coursed among RAHy and RBHy, and were located dorsally to Shh-immunoreactivity (I,J). Note the presence of 5-HT-ir fibers in the Sp (I,J,L). The white arrowhead in (J,K) points to 5-HT-ir fibers that course in the rostral CAHy. The black arrowhead in (J,L) points to 5-HT-ir fibers in the telencephalon. The arrow in (J,K) points to 5-HT-ir fibers decussating in the CBHy. The arrow in (L) points to the faint Shh immunoreactivity in the zli. (M,N) Shh IHC combined with ScDlx2/5 expression (M) or ScOtp expression (N). A gap of expression is observed between the rostral and caudal domains of ScDlx2/5 and ScOtp expression, which appeared to coincide with the path followed by 5-HT-ir fibers. (O) GFAP-ir processes at the level shown in (J). The arrowhead points to the GFAP-ir processes among RAHy and Sp. The arrow points to the GFAP-ir processes in the CBHy. (P) GFAP-ir processes at the level shown in (J). The arrow points to GFAP-ir processes in the Sp. For abbreviations, see list.
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Figure 4: Regionalization of the shark hypothalamus from stages 29–31 based on immunoreactivity to Shh (A,B,B′,D,I–N), TH (B′), 5-HT (I–L), GFAP (O, P) and expression of ScNkx2.1 (C,C′,D,G″), ScDlx2/5(E,E′,F,M) and ScOtp(G,G′, G″, H, H′, N) genes by means of single immunohistochemistry (IHC; A,B,O,P), double IHC (B′,I–L), single ISH (C,E,E′,F,G, G′,H,H′) and/or combined with IHC (D,M,N) on sagittal (A,B,B′,C–G,G″,H–J,M,N) or transverse sections (C′,E′,G′,H′,K,L,O,P). Image in (G″) results from the overlapping of two parallel sections respectively hybridized with ScOtp and ScNkx2.1 probes. Color for ScNkx2.1 was digitally converted to brown to ease comparison. Dotted lines define the hypothalamo-telencephalic boundary (HTB), dashed lines indicate the caudal border of the secondary prosencephalon, red lines indicate the ABB and continuous black lines represent the path followed by 5-HT-ir fibers. (A) Shh-immunoreactivity was observed in the most caudo-ventral part of the CBHy (arrow) and in the RBHy. The arrowhead points to the zli. (B) Shh-immunoreactivity was observed in the telencephalon (arrowhead) beyond the territory of the anterior commissure (asterisk). The arrow points to Shh-immunoreactivity in the caudal-most CBHy. (B′) Detail of the squared area in (B) to show Shh- and TH-immunoreactivity in its most caudo-ventral part (arrow). (C,D)ScNkx2.1 expression was observed in the hypothalamus and telencephalon. A detail of a transverse section at the level indicated in (C) is shown in (C′). The arrows in (C,C′,D) point to ScNkx2.1-expressing cells in the mantle zone of the most caudo-ventral CBHy. The arrowheads in (C,D) indicate a wedge-shaped domain lacking ScNkx2.1 expression. The asterisk in (D) indicates the territory of the anterior commissure. (E,F)ScDlx2/5 expression was observed in p3 and in the secondary prosencephalon. A detail of a transverse section at the level indicated in (D) is shown in (D′). The arrow in (E,E′) points to ScDlx2/5-expressing cells in the mantle of the p3Tg. The star in (E,E′) indicates the prospective territory of the PThE. The black asterisks in (E,F) indicate a gap of ScDlx2/5 expression in the telencephalon. The arrowheads in (E,F) point to ScDlx2/5 expression in the BHy. (G,H)ScOtp expression in the hypothalamus. Details in (G′,H′) correspond to transverse sections at the levels indicated in (G,H). Detail in (G″) correspond to the squared area in (G). The arrows in (G,G″) point to the ventricular domain expressing ScOtp in the caudal CBHy. The black arrowheads in (G,G″, H′) point to ScOtp-expressing cells in the mantle of the most caudo-ventral part of CBHy and p3Tg. The arrow in (G″) indicates a domain expressing ScNkx2.1 alone. The white asterisks in (G′,H) indicate ScOtp-expressing cells in the mantle zone. The black arrowhead in (H) points to ScOtp-expressing cells in the AHy and the white arrowhead in (H) points to ScOtp-expressing cells between the alar and basal domains. (I–L) Double Shh- and 5-HT-immunoreactivity. (K,L) correspond to trasverse sections at the level indicated in (J). 5-HT-ir fibers in (I) are observed in the basal plate of the secondary prosencephalon. In the rostral hypothalamus such fibers coursed among RAHy and RBHy, and were located dorsally to Shh-immunoreactivity (I,J). Note the presence of 5-HT-ir fibers in the Sp (I,J,L). The white arrowhead in (J,K) points to 5-HT-ir fibers that course in the rostral CAHy. The black arrowhead in (J,L) points to 5-HT-ir fibers in the telencephalon. The arrow in (J,K) points to 5-HT-ir fibers decussating in the CBHy. The arrow in (L) points to the faint Shh immunoreactivity in the zli. (M,N) Shh IHC combined with ScDlx2/5 expression (M) or ScOtp expression (N). A gap of expression is observed between the rostral and caudal domains of ScDlx2/5 and ScOtp expression, which appeared to coincide with the path followed by 5-HT-ir fibers. (O) GFAP-ir processes at the level shown in (J). The arrowhead points to the GFAP-ir processes among RAHy and Sp. The arrow points to the GFAP-ir processes in the CBHy. (P) GFAP-ir processes at the level shown in (J). The arrow points to GFAP-ir processes in the Sp. For abbreviations, see list.
Mentions: ScShh expression was detected during gastrulation (stage 12) in the caudal midline of the embryo (data not shown). At stage 14, during early neurulation, it has been detected in the axial mesoderm of the notochord and the prechordal plate and in the ectoderm of the caudal midline (data not shown). After the closure of the neural tube (stage 17), the signal was detected as a ventral longitudinal continuous band that extends from the caudal end of the spinal cord to the At of the forebrain, roughly at the level of the optic stalk (Figure 3D). As in other vertebrates (Shimamura et al., 1995), the expression of ScShh can be used to define the alar-basal boundary (ABB; Figures 3E–H). At stage 19, ScShh expression became downregulated in the forebrain to progressively give rise to a caudal and a rostral domain (arrow in Figures 3E–H). The narrow transverse and dorsally directed stripe of ScShh-expressing cells within the caudal domain was identified as the developing zona limitans intrathalamica (zli; arrowhead in Figure 3G). The rostral border of the ScShh caudal domain, in turn, was somewhat extended rostral to the HDB (Puelles et al., 2012), which at this stage was identified as the point where the neural tube expands to acquire the distinctive shape of the ventral hypothalamus. Therefore, the BHy appeared to be divided in three domains: two positive for ScShh (one rostral and other caudal) and one (intermediate) negative for ScShh (arrow in Figures 3G,H; see also Figure 5H in Compagnucci et al., 2013). Of note, the dorsal border of the rostral domain (presumably corresponding to the ABB) seems to codistribute with α-acetylated-tubulin-immunoreactive (-ir) longitudinal tracts (arrowheads in Figure 3I). At stage 24 (Figure 3H), a new domain emerged within the telencephalon. This short domain (arrowhead in Figure 3H) extended from a region located dorsally to the optic stalk without reaching the prospective territory of the anterior commissure (that can be identified at early development by means of α-tubulin-immunoreactivity; asterisk in Figures 3H,I). A clear gap of expression was observed between this telencephalic domain and the rostral hypothalamic one (Figure 3H). The telencephalic domain was located medially while the hypothalamic one also expanded laterally (not shown). From stage 27 onward the zli expanded dorsally toward the roof plate (arrowhead in Figure 4A). At stage 29 the medio-lateral histologic organization of the developing walls of the forebrain become more evident. As in previous developmental stages, Shh immunoreactivity was clearly identified in the basal plate of the diencephalon entering the caudo-ventral part of the BHy (arrow in Figures 4A,B,B′) and in the rostro-dorsal part of the BHy (Figures 4A,B), so that a clear negative gap of Shh-immunoreactivity occupied most of the caudal BHy (CBHy; Figures 4A,B) and part of the rostral BHy (RBHy). In the telencephalon, Shh-immunoreactivity expanded caudally beyond the prospective territory of the anterior commissure (arrowhead in Figure 4B; compare with Figure 3H). Of note, from late stage 30 onward, Shh-immunoreactivity is downregulated in the CBHy and basal diencephalon, except in the zli (data not shown).

Bottom Line: Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain.Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates.These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

View Article: PubMed Central - PubMed

Affiliation: Centro de Investigaciones Biológicas, Department of Cell Biology and Ecology, University of Santiago de Compostela Santiago de Compostela, Spain.

ABSTRACT
The hypothalamus has been a central topic in neuroanatomy because of its important physiological functions, but its mature organization remains elusive. Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain. Here we studied the molecular organization of the hypothalamus and neighboring telencephalic domains in a cartilaginous fish, the catshark, Scyliorhinus canicula, focusing on ScFoxg1a, ScShh, ScNkx2.1, ScDlx2/5, ScOtp, and ScTbr1 expression profiles and on the identification α-acetylated-tubulin-immunoreactive (ir), TH-ir, 5-HT-ir, and GFAP-ir structures by means of immunohistochemistry. Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates. These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

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