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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.

No MeSH data available.


Related in: MedlinePlus

Regionalization of the hypothalamus and neighbor territories in embryos of S. canicula from stages 18–29 based on the expression pattern of ScFoxg1a(A–C), ScShh(D–H), ScNkx2.1(J–L), ScDlx5(M–O), ScOtp(P,Q), ScTbr1(R) genes and α-acetylated-tubulin immunoreactivity (I). In all panels, dotted lines define the hypothalamo-telencephalic boundary (HTB), dashed lines indicate the caudal border of the secondary prosencephalon and red lines indicate the ABB. (A–C)ScFoxg1a expression in the secondary prosencephalon at indicated stages. The arrowheads in (A) mark the caudo-dorsal and rostro-ventral limit of ScFoxg1a expression. (D–H)ScShh expression at the indicated stages. The arrowhead in (D) marks the rostral-most point of ScShh expression in the forebrain. The arrows in (E–H) indicate the downregulation of ScShh expression in the hypothalamus. The arrowhead in (G) points to the developing zli. The arrowhead in (H) points to a novel domain in the telencephalon. The asterisk in (H) marks the prospective territory of the anterior commissure. (I) Anti-α-acetylated-tubulin IHC to show three sets of tracts at stage 25. These tracts are classically referred as sot, TPOC and MTT. The asterisk indicates the territory of the developing anterior commissure. The arrowheads point to the longitudinal TPOC. The arrow points to the rostral-most extension of the MTT. (J–L)ScNkx2.1 expression at the indicated stages. The arrowhead in (J) points to the rostral-most point of ScNkx2.1 expression at stage 18, which was restricted to a short longitudinal domain ventrally to the optic stalk. The arrow in (K,L) points to a small ScNkx2.1-negative domain at the most caudo-ventral BHy. The asterisk in (K,L) marks the prospective territory of the anterior commissure. The arrowhead in (K,L) points to a domain in the telencephalon that spread rostro-caudally. (M–O)ScDlx5 expression at the indicated stages. The arrowheads in (M,N) indicate ScDlx5 expression in the olfactory placode and the anterior part of the telencephalon. The asterisk in (N) indicates the prospective territory of the anterior commissure. The arrowheads in (O) point to the ventral and caudal expansion of ScDlx5 expression in the telencephalon. This domain was fairly continuous with a longitudinal band of ScDlx5 over the ABB. The arrows in (O) point to ScDlx5-expressing domains that spread into the BHy. (P,Q)ScOtp expression at the indicated stages. The arrowhead in (P) indicates a restricted domain of ScOtp expression ventrally located with respect to the optic stalk. The expression of ScOtp in the hypothalamus was faint compared to that of the Rh. The white arrowhead in (Q) points to ScOtp expression in the AHy. Two additional ScOtp-expressing domains were observed in the BHy. (R)ScTbr1 expression at stage 25 was found in part of the telencephalon and at the dorsal-most part of the rostral diencephalon (white arrowhead). The asterisk indicates the prospective territory of the anterior commissure. For abbreviations, see list.
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Figure 3: Regionalization of the hypothalamus and neighbor territories in embryos of S. canicula from stages 18–29 based on the expression pattern of ScFoxg1a(A–C), ScShh(D–H), ScNkx2.1(J–L), ScDlx5(M–O), ScOtp(P,Q), ScTbr1(R) genes and α-acetylated-tubulin immunoreactivity (I). In all panels, dotted lines define the hypothalamo-telencephalic boundary (HTB), dashed lines indicate the caudal border of the secondary prosencephalon and red lines indicate the ABB. (A–C)ScFoxg1a expression in the secondary prosencephalon at indicated stages. The arrowheads in (A) mark the caudo-dorsal and rostro-ventral limit of ScFoxg1a expression. (D–H)ScShh expression at the indicated stages. The arrowhead in (D) marks the rostral-most point of ScShh expression in the forebrain. The arrows in (E–H) indicate the downregulation of ScShh expression in the hypothalamus. The arrowhead in (G) points to the developing zli. The arrowhead in (H) points to a novel domain in the telencephalon. The asterisk in (H) marks the prospective territory of the anterior commissure. (I) Anti-α-acetylated-tubulin IHC to show three sets of tracts at stage 25. These tracts are classically referred as sot, TPOC and MTT. The asterisk indicates the territory of the developing anterior commissure. The arrowheads point to the longitudinal TPOC. The arrow points to the rostral-most extension of the MTT. (J–L)ScNkx2.1 expression at the indicated stages. The arrowhead in (J) points to the rostral-most point of ScNkx2.1 expression at stage 18, which was restricted to a short longitudinal domain ventrally to the optic stalk. The arrow in (K,L) points to a small ScNkx2.1-negative domain at the most caudo-ventral BHy. The asterisk in (K,L) marks the prospective territory of the anterior commissure. The arrowhead in (K,L) points to a domain in the telencephalon that spread rostro-caudally. (M–O)ScDlx5 expression at the indicated stages. The arrowheads in (M,N) indicate ScDlx5 expression in the olfactory placode and the anterior part of the telencephalon. The asterisk in (N) indicates the prospective territory of the anterior commissure. The arrowheads in (O) point to the ventral and caudal expansion of ScDlx5 expression in the telencephalon. This domain was fairly continuous with a longitudinal band of ScDlx5 over the ABB. The arrows in (O) point to ScDlx5-expressing domains that spread into the BHy. (P,Q)ScOtp expression at the indicated stages. The arrowhead in (P) indicates a restricted domain of ScOtp expression ventrally located with respect to the optic stalk. The expression of ScOtp in the hypothalamus was faint compared to that of the Rh. The white arrowhead in (Q) points to ScOtp expression in the AHy. Two additional ScOtp-expressing domains were observed in the BHy. (R)ScTbr1 expression at stage 25 was found in part of the telencephalon and at the dorsal-most part of the rostral diencephalon (white arrowhead). The asterisk indicates the prospective territory of the anterior commissure. For abbreviations, see list.

Mentions: In mice, Foxg1 is one of the earliest transcription factors expressed specifically in the part of the neural plate that gives rise to the telencephalon and it remains expressed throughout the telencephalon during embryonic development (see Manuel et al., 2011). In an attempt to discriminate telencephalic and underlying hypothalamic domains throughout S. canicula development, we have analyzed the expression of ScFoxg1a in the developing nervous system of this species. At stage 18, ScFoxg1a expression was found in the dorsal-most portion of the secondary prosencephalon including the optic cup, extending from the level of the optic stalk (which is located rostrally, within the At) up to a caudal point in the roof plate, which has been tentatively identified as the dorsal border between the telencephalon and the diencephalon (Figure 3A). At stage 22, ScFoxg1a was observed in the telencephalon and in the nasal part of the optic cup (Figure 3B). The expression in the telencephalon was maintained until late stages of development (Figure 3C), which allowed identifying the border between the telencephalon and the hypothalamus.


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 hypothalamus and neighbor territories in embryos of S. canicula from stages 18–29 based on the expression pattern of ScFoxg1a(A–C), ScShh(D–H), ScNkx2.1(J–L), ScDlx5(M–O), ScOtp(P,Q), ScTbr1(R) genes and α-acetylated-tubulin immunoreactivity (I). In all panels, dotted lines define the hypothalamo-telencephalic boundary (HTB), dashed lines indicate the caudal border of the secondary prosencephalon and red lines indicate the ABB. (A–C)ScFoxg1a expression in the secondary prosencephalon at indicated stages. The arrowheads in (A) mark the caudo-dorsal and rostro-ventral limit of ScFoxg1a expression. (D–H)ScShh expression at the indicated stages. The arrowhead in (D) marks the rostral-most point of ScShh expression in the forebrain. The arrows in (E–H) indicate the downregulation of ScShh expression in the hypothalamus. The arrowhead in (G) points to the developing zli. The arrowhead in (H) points to a novel domain in the telencephalon. The asterisk in (H) marks the prospective territory of the anterior commissure. (I) Anti-α-acetylated-tubulin IHC to show three sets of tracts at stage 25. These tracts are classically referred as sot, TPOC and MTT. The asterisk indicates the territory of the developing anterior commissure. The arrowheads point to the longitudinal TPOC. The arrow points to the rostral-most extension of the MTT. (J–L)ScNkx2.1 expression at the indicated stages. The arrowhead in (J) points to the rostral-most point of ScNkx2.1 expression at stage 18, which was restricted to a short longitudinal domain ventrally to the optic stalk. The arrow in (K,L) points to a small ScNkx2.1-negative domain at the most caudo-ventral BHy. The asterisk in (K,L) marks the prospective territory of the anterior commissure. The arrowhead in (K,L) points to a domain in the telencephalon that spread rostro-caudally. (M–O)ScDlx5 expression at the indicated stages. The arrowheads in (M,N) indicate ScDlx5 expression in the olfactory placode and the anterior part of the telencephalon. The asterisk in (N) indicates the prospective territory of the anterior commissure. The arrowheads in (O) point to the ventral and caudal expansion of ScDlx5 expression in the telencephalon. This domain was fairly continuous with a longitudinal band of ScDlx5 over the ABB. The arrows in (O) point to ScDlx5-expressing domains that spread into the BHy. (P,Q)ScOtp expression at the indicated stages. The arrowhead in (P) indicates a restricted domain of ScOtp expression ventrally located with respect to the optic stalk. The expression of ScOtp in the hypothalamus was faint compared to that of the Rh. The white arrowhead in (Q) points to ScOtp expression in the AHy. Two additional ScOtp-expressing domains were observed in the BHy. (R)ScTbr1 expression at stage 25 was found in part of the telencephalon and at the dorsal-most part of the rostral diencephalon (white arrowhead). The asterisk indicates the prospective territory of the anterior commissure. For abbreviations, see list.
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Figure 3: Regionalization of the hypothalamus and neighbor territories in embryos of S. canicula from stages 18–29 based on the expression pattern of ScFoxg1a(A–C), ScShh(D–H), ScNkx2.1(J–L), ScDlx5(M–O), ScOtp(P,Q), ScTbr1(R) genes and α-acetylated-tubulin immunoreactivity (I). In all panels, dotted lines define the hypothalamo-telencephalic boundary (HTB), dashed lines indicate the caudal border of the secondary prosencephalon and red lines indicate the ABB. (A–C)ScFoxg1a expression in the secondary prosencephalon at indicated stages. The arrowheads in (A) mark the caudo-dorsal and rostro-ventral limit of ScFoxg1a expression. (D–H)ScShh expression at the indicated stages. The arrowhead in (D) marks the rostral-most point of ScShh expression in the forebrain. The arrows in (E–H) indicate the downregulation of ScShh expression in the hypothalamus. The arrowhead in (G) points to the developing zli. The arrowhead in (H) points to a novel domain in the telencephalon. The asterisk in (H) marks the prospective territory of the anterior commissure. (I) Anti-α-acetylated-tubulin IHC to show three sets of tracts at stage 25. These tracts are classically referred as sot, TPOC and MTT. The asterisk indicates the territory of the developing anterior commissure. The arrowheads point to the longitudinal TPOC. The arrow points to the rostral-most extension of the MTT. (J–L)ScNkx2.1 expression at the indicated stages. The arrowhead in (J) points to the rostral-most point of ScNkx2.1 expression at stage 18, which was restricted to a short longitudinal domain ventrally to the optic stalk. The arrow in (K,L) points to a small ScNkx2.1-negative domain at the most caudo-ventral BHy. The asterisk in (K,L) marks the prospective territory of the anterior commissure. The arrowhead in (K,L) points to a domain in the telencephalon that spread rostro-caudally. (M–O)ScDlx5 expression at the indicated stages. The arrowheads in (M,N) indicate ScDlx5 expression in the olfactory placode and the anterior part of the telencephalon. The asterisk in (N) indicates the prospective territory of the anterior commissure. The arrowheads in (O) point to the ventral and caudal expansion of ScDlx5 expression in the telencephalon. This domain was fairly continuous with a longitudinal band of ScDlx5 over the ABB. The arrows in (O) point to ScDlx5-expressing domains that spread into the BHy. (P,Q)ScOtp expression at the indicated stages. The arrowhead in (P) indicates a restricted domain of ScOtp expression ventrally located with respect to the optic stalk. The expression of ScOtp in the hypothalamus was faint compared to that of the Rh. The white arrowhead in (Q) points to ScOtp expression in the AHy. Two additional ScOtp-expressing domains were observed in the BHy. (R)ScTbr1 expression at stage 25 was found in part of the telencephalon and at the dorsal-most part of the rostral diencephalon (white arrowhead). The asterisk indicates the prospective territory of the anterior commissure. For abbreviations, see list.
Mentions: In mice, Foxg1 is one of the earliest transcription factors expressed specifically in the part of the neural plate that gives rise to the telencephalon and it remains expressed throughout the telencephalon during embryonic development (see Manuel et al., 2011). In an attempt to discriminate telencephalic and underlying hypothalamic domains throughout S. canicula development, we have analyzed the expression of ScFoxg1a in the developing nervous system of this species. At stage 18, ScFoxg1a expression was found in the dorsal-most portion of the secondary prosencephalon including the optic cup, extending from the level of the optic stalk (which is located rostrally, within the At) up to a caudal point in the roof plate, which has been tentatively identified as the dorsal border between the telencephalon and the diencephalon (Figure 3A). At stage 22, ScFoxg1a was observed in the telencephalon and in the nasal part of the optic cup (Figure 3B). The expression in the telencephalon was maintained until late stages of development (Figure 3C), which allowed identifying the border between the telencephalon and the hypothalamus.

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.

No MeSH data available.


Related in: MedlinePlus