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Molecular codes defining rostrocaudal domains in the embryonic mouse hypothalamus.

Ferran JL, Puelles L, Rubenstein JL - Front Neuroanat (2015)

Bottom Line: A number of markers were expressed in Thy (Fgf15, Gsc, Nkx6.2, Otx1, Zic1/5), but were absent in PHy, while other genes showed the converse pattern (Erbb4, Irx1/3/5, Lmo4, Mfap4, Plagl1, Pmch).We also identified markers that selectively label the ATD (Fgf8/10/18, Otx2, Pomc, Rax, Six6).On the whole, these data help to explain why, irrespective of the observed continuity of all dorsoventral molecular hypothalamic subdivisions across PHy and THy, different nuclear structures originate within each of these two domains, and also why singular structures arise at the ATD, e.g., the suprachiasmatic nuclei, the arcuate nucleus, the median eminence and the neurohypophysis.

View Article: PubMed Central - PubMed

Affiliation: Department of Human Anatomy and Psychobiology, School Medicine, University of Murcia and IMIB (Instituto Murciano de Investigación Biosanitaria) Murcia, Spain.

ABSTRACT
The prosomeric model proposes that the hypothalamus is a rostral forebrain entity, placed ventral to the telencephalon and rostral to the diencephalon. Gene expression markers differentially label molecularly distinct dorsoventral progenitor domains, which represent continuous longitudinal bands across the hypothalamic alar and basal regions. There is also circumstantial support for a rostrocaudal subdivision of the hypothalamus into transverse peduncular (caudal) and terminal (rostral) territories (PHy, THy). In addition, there is evidence for a specialized acroterminal domain at the rostral midline of the terminal hypothalamus (ATD). The PHy and THy transverse structural units are presently held to form part of two hypothalamo-telencephalic prosomeres (hp1 and hp2, respectively), which end dorsally at the telencephalic septocommissural roof. PHy and THy have distinct adult nuclei, at all dorsoventral levels. Here we report the results of data mining from the Allen Developing Mouse Brain Atlas database, looking for genes expressed differentially in the PHy, Thy, and ATD regions of the hypothalamus at several developmental stages. This search allowed us to identify additional molecular evidence supporting the postulated fundamental rostrocaudal bipartition of the mouse hypothalamus into the PHy and THy, and also corroborated molecularly the singularity of the ATD. A number of markers were expressed in Thy (Fgf15, Gsc, Nkx6.2, Otx1, Zic1/5), but were absent in PHy, while other genes showed the converse pattern (Erbb4, Irx1/3/5, Lmo4, Mfap4, Plagl1, Pmch). We also identified markers that selectively label the ATD (Fgf8/10/18, Otx2, Pomc, Rax, Six6). On the whole, these data help to explain why, irrespective of the observed continuity of all dorsoventral molecular hypothalamic subdivisions across PHy and THy, different nuclear structures originate within each of these two domains, and also why singular structures arise at the ATD, e.g., the suprachiasmatic nuclei, the arcuate nucleus, the median eminence and the neurohypophysis.

No MeSH data available.


Related in: MedlinePlus

Schemata representing the updated prosomeric model of the forebrain (excepting diencephalic p1), in which the general position, morphological organization and principal nuclear and genoarchitectonic subdivisions of the hypothalamus are detailed. (A) Schema showing the two rostral diencephalic prosomeres (p2 and p3) and the hypothalamo-telencephalic prosomeres 1 and 2 (hp1 and hp2). Note hp1 contains the peduncular hypothalamic region (PHy), whereas hp2 includes the terminal hypothalamic region (THy) and the rostralmost, median acroterminal domain (ATHy). (B) Schema of the main hypothalamic progenitor areas distributed across the dorsoventral and anteroposterior dimensions. The longitudinal alar/basal boundary (ABb) is indicated as a thick dark line. The hypothalamic area is subdivided rostrocaudally into neuromeric THy and PHy parts (pink and green, respectively). Alar territories (AP) are shown on the left, and basal ones on the right. The alar hypothalamus is subdivided dorsoventrally into paraventricular (TPa/PPa) and subparaventricular (TSPa, PsPa) areas, plus the corresponding acroterminal domains. The paraventricular area shows a general tripartition into dorsal, central and ventral subdivisions (DPa, CPa, VPa). The basal hypothalamus is also subdivided dorsoventrally into the large tuberal/retrotuberal (Tu/RTu) area and the primary mamillary/retromamillary (M/RM) area, plus the corresponding acroterminal regions. The THy/PHy parts of the hypothalamic floor lie underneath (FP). Moreover, the Tu/RTu region is subdivided into three dorsoventral parts: TuD/RTuD, TuI/RTuI, and TuV/RTuV, and the primary M/RM area is subdivided into perimamillary/periretromamillary area (PM/PRM) and the secondary M/RM area. Some well-known nuclear elements of the hypothalamus are represented within their respective topography relative to the molecular domains; note some of these positions are postmigratory (see the list for abbreviations).
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Figure 1: Schemata representing the updated prosomeric model of the forebrain (excepting diencephalic p1), in which the general position, morphological organization and principal nuclear and genoarchitectonic subdivisions of the hypothalamus are detailed. (A) Schema showing the two rostral diencephalic prosomeres (p2 and p3) and the hypothalamo-telencephalic prosomeres 1 and 2 (hp1 and hp2). Note hp1 contains the peduncular hypothalamic region (PHy), whereas hp2 includes the terminal hypothalamic region (THy) and the rostralmost, median acroterminal domain (ATHy). (B) Schema of the main hypothalamic progenitor areas distributed across the dorsoventral and anteroposterior dimensions. The longitudinal alar/basal boundary (ABb) is indicated as a thick dark line. The hypothalamic area is subdivided rostrocaudally into neuromeric THy and PHy parts (pink and green, respectively). Alar territories (AP) are shown on the left, and basal ones on the right. The alar hypothalamus is subdivided dorsoventrally into paraventricular (TPa/PPa) and subparaventricular (TSPa, PsPa) areas, plus the corresponding acroterminal domains. The paraventricular area shows a general tripartition into dorsal, central and ventral subdivisions (DPa, CPa, VPa). The basal hypothalamus is also subdivided dorsoventrally into the large tuberal/retrotuberal (Tu/RTu) area and the primary mamillary/retromamillary (M/RM) area, plus the corresponding acroterminal regions. The THy/PHy parts of the hypothalamic floor lie underneath (FP). Moreover, the Tu/RTu region is subdivided into three dorsoventral parts: TuD/RTuD, TuI/RTuI, and TuV/RTuV, and the primary M/RM area is subdivided into perimamillary/periretromamillary area (PM/PRM) and the secondary M/RM area. Some well-known nuclear elements of the hypothalamus are represented within their respective topography relative to the molecular domains; note some of these positions are postmigratory (see the list for abbreviations).

Mentions: However, conventional analysis of nuclear structure in the hypothalamus already underlines the existence of grisea that apparently only develop within the rostral or caudal moieties of the cited longitudinal bands. Clearcut examples of this are the anterolateral, suprachiasmatic, anterior, ventromedial, ventral/dorsal premamillary and arcuate nuclei, only present rostrally, and the main paraventricular nucleus, jointly with the entopeduncular nuclei and the subthalamic nucleus, only present caudally. Moreover, distinct mamillary (rostral) and retromamillary (caudal) formations have been distinguished within the mamillary region. Such differences already suggested an anteroposterior bipartition of the hypothalamus (Puelles and Rubenstein, 2003; Puelles et al., 2012) finally postulated that such bipartition responded to the existence of two distinct neuromeric fields stretching through the hypothalamus and telencephalon continuum (hypothalamic prosomeres hp1 and hp2, named in caudorostral order) (Figure 1A). The corresponding hypothalamic parts were identified as peduncular and terminal hypothalamus (PHy, THy; note there is a rough correspondence of these transverse parts with historical use by Herrick, 1910 and others of the notion of “dorsal” and “ventral” hypothalamus, of course referring to a completely different length axis; this use has been abandoned by columnar authors in recent times, e.g., see Swanson, 1992, 2003; other authors identified THy as “hypothalamus” and PHy as “subthalamus,” e.g., Reinoso-Suárez, 1960; Richter, 1965; see discussion in Puelles et al., 2012).


Molecular codes defining rostrocaudal domains in the embryonic mouse hypothalamus.

Ferran JL, Puelles L, Rubenstein JL - Front Neuroanat (2015)

Schemata representing the updated prosomeric model of the forebrain (excepting diencephalic p1), in which the general position, morphological organization and principal nuclear and genoarchitectonic subdivisions of the hypothalamus are detailed. (A) Schema showing the two rostral diencephalic prosomeres (p2 and p3) and the hypothalamo-telencephalic prosomeres 1 and 2 (hp1 and hp2). Note hp1 contains the peduncular hypothalamic region (PHy), whereas hp2 includes the terminal hypothalamic region (THy) and the rostralmost, median acroterminal domain (ATHy). (B) Schema of the main hypothalamic progenitor areas distributed across the dorsoventral and anteroposterior dimensions. The longitudinal alar/basal boundary (ABb) is indicated as a thick dark line. The hypothalamic area is subdivided rostrocaudally into neuromeric THy and PHy parts (pink and green, respectively). Alar territories (AP) are shown on the left, and basal ones on the right. The alar hypothalamus is subdivided dorsoventrally into paraventricular (TPa/PPa) and subparaventricular (TSPa, PsPa) areas, plus the corresponding acroterminal domains. The paraventricular area shows a general tripartition into dorsal, central and ventral subdivisions (DPa, CPa, VPa). The basal hypothalamus is also subdivided dorsoventrally into the large tuberal/retrotuberal (Tu/RTu) area and the primary mamillary/retromamillary (M/RM) area, plus the corresponding acroterminal regions. The THy/PHy parts of the hypothalamic floor lie underneath (FP). Moreover, the Tu/RTu region is subdivided into three dorsoventral parts: TuD/RTuD, TuI/RTuI, and TuV/RTuV, and the primary M/RM area is subdivided into perimamillary/periretromamillary area (PM/PRM) and the secondary M/RM area. Some well-known nuclear elements of the hypothalamus are represented within their respective topography relative to the molecular domains; note some of these positions are postmigratory (see the list for abbreviations).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400913&req=5

Figure 1: Schemata representing the updated prosomeric model of the forebrain (excepting diencephalic p1), in which the general position, morphological organization and principal nuclear and genoarchitectonic subdivisions of the hypothalamus are detailed. (A) Schema showing the two rostral diencephalic prosomeres (p2 and p3) and the hypothalamo-telencephalic prosomeres 1 and 2 (hp1 and hp2). Note hp1 contains the peduncular hypothalamic region (PHy), whereas hp2 includes the terminal hypothalamic region (THy) and the rostralmost, median acroterminal domain (ATHy). (B) Schema of the main hypothalamic progenitor areas distributed across the dorsoventral and anteroposterior dimensions. The longitudinal alar/basal boundary (ABb) is indicated as a thick dark line. The hypothalamic area is subdivided rostrocaudally into neuromeric THy and PHy parts (pink and green, respectively). Alar territories (AP) are shown on the left, and basal ones on the right. The alar hypothalamus is subdivided dorsoventrally into paraventricular (TPa/PPa) and subparaventricular (TSPa, PsPa) areas, plus the corresponding acroterminal domains. The paraventricular area shows a general tripartition into dorsal, central and ventral subdivisions (DPa, CPa, VPa). The basal hypothalamus is also subdivided dorsoventrally into the large tuberal/retrotuberal (Tu/RTu) area and the primary mamillary/retromamillary (M/RM) area, plus the corresponding acroterminal regions. The THy/PHy parts of the hypothalamic floor lie underneath (FP). Moreover, the Tu/RTu region is subdivided into three dorsoventral parts: TuD/RTuD, TuI/RTuI, and TuV/RTuV, and the primary M/RM area is subdivided into perimamillary/periretromamillary area (PM/PRM) and the secondary M/RM area. Some well-known nuclear elements of the hypothalamus are represented within their respective topography relative to the molecular domains; note some of these positions are postmigratory (see the list for abbreviations).
Mentions: However, conventional analysis of nuclear structure in the hypothalamus already underlines the existence of grisea that apparently only develop within the rostral or caudal moieties of the cited longitudinal bands. Clearcut examples of this are the anterolateral, suprachiasmatic, anterior, ventromedial, ventral/dorsal premamillary and arcuate nuclei, only present rostrally, and the main paraventricular nucleus, jointly with the entopeduncular nuclei and the subthalamic nucleus, only present caudally. Moreover, distinct mamillary (rostral) and retromamillary (caudal) formations have been distinguished within the mamillary region. Such differences already suggested an anteroposterior bipartition of the hypothalamus (Puelles and Rubenstein, 2003; Puelles et al., 2012) finally postulated that such bipartition responded to the existence of two distinct neuromeric fields stretching through the hypothalamus and telencephalon continuum (hypothalamic prosomeres hp1 and hp2, named in caudorostral order) (Figure 1A). The corresponding hypothalamic parts were identified as peduncular and terminal hypothalamus (PHy, THy; note there is a rough correspondence of these transverse parts with historical use by Herrick, 1910 and others of the notion of “dorsal” and “ventral” hypothalamus, of course referring to a completely different length axis; this use has been abandoned by columnar authors in recent times, e.g., see Swanson, 1992, 2003; other authors identified THy as “hypothalamus” and PHy as “subthalamus,” e.g., Reinoso-Suárez, 1960; Richter, 1965; see discussion in Puelles et al., 2012).

Bottom Line: A number of markers were expressed in Thy (Fgf15, Gsc, Nkx6.2, Otx1, Zic1/5), but were absent in PHy, while other genes showed the converse pattern (Erbb4, Irx1/3/5, Lmo4, Mfap4, Plagl1, Pmch).We also identified markers that selectively label the ATD (Fgf8/10/18, Otx2, Pomc, Rax, Six6).On the whole, these data help to explain why, irrespective of the observed continuity of all dorsoventral molecular hypothalamic subdivisions across PHy and THy, different nuclear structures originate within each of these two domains, and also why singular structures arise at the ATD, e.g., the suprachiasmatic nuclei, the arcuate nucleus, the median eminence and the neurohypophysis.

View Article: PubMed Central - PubMed

Affiliation: Department of Human Anatomy and Psychobiology, School Medicine, University of Murcia and IMIB (Instituto Murciano de Investigación Biosanitaria) Murcia, Spain.

ABSTRACT
The prosomeric model proposes that the hypothalamus is a rostral forebrain entity, placed ventral to the telencephalon and rostral to the diencephalon. Gene expression markers differentially label molecularly distinct dorsoventral progenitor domains, which represent continuous longitudinal bands across the hypothalamic alar and basal regions. There is also circumstantial support for a rostrocaudal subdivision of the hypothalamus into transverse peduncular (caudal) and terminal (rostral) territories (PHy, THy). In addition, there is evidence for a specialized acroterminal domain at the rostral midline of the terminal hypothalamus (ATD). The PHy and THy transverse structural units are presently held to form part of two hypothalamo-telencephalic prosomeres (hp1 and hp2, respectively), which end dorsally at the telencephalic septocommissural roof. PHy and THy have distinct adult nuclei, at all dorsoventral levels. Here we report the results of data mining from the Allen Developing Mouse Brain Atlas database, looking for genes expressed differentially in the PHy, Thy, and ATD regions of the hypothalamus at several developmental stages. This search allowed us to identify additional molecular evidence supporting the postulated fundamental rostrocaudal bipartition of the mouse hypothalamus into the PHy and THy, and also corroborated molecularly the singularity of the ATD. A number of markers were expressed in Thy (Fgf15, Gsc, Nkx6.2, Otx1, Zic1/5), but were absent in PHy, while other genes showed the converse pattern (Erbb4, Irx1/3/5, Lmo4, Mfap4, Plagl1, Pmch). We also identified markers that selectively label the ATD (Fgf8/10/18, Otx2, Pomc, Rax, Six6). On the whole, these data help to explain why, irrespective of the observed continuity of all dorsoventral molecular hypothalamic subdivisions across PHy and THy, different nuclear structures originate within each of these two domains, and also why singular structures arise at the ATD, e.g., the suprachiasmatic nuclei, the arcuate nucleus, the median eminence and the neurohypophysis.

No MeSH data available.


Related in: MedlinePlus