The distribution of GAD67-mRNA in the adult zebrafish (teleost) forebrain reveals a prosomeric pattern and suggests previously unidentified homologies to tetrapods - PubMed (original) (raw)
The distribution of GAD67-mRNA in the adult zebrafish (teleost) forebrain reveals a prosomeric pattern and suggests previously unidentified homologies to tetrapods
Thomas Mueller et al. J Comp Neurol. 2009.
Abstract
We used in situ hybridization on sections to examine the distribution of GAD67-expressing cell populations in the entire forebrain of the adult zebrafish. GAD67 is predominantly expressed in the olfactory bulb (OB), all regions of the subpallium (including the dorsal, ventral, central, and lateral nucleus of the area ventralis [Vd, Vv, Vc, and Vl, respectively]), as well as preoptic (PPa, PPp, and PM), pretectal (PPd, PPv, PCN, PSp, and PSm), ventral (= pre-) thalamic (I, VM, and VL), hypothalamic (Hr, Hi, and Hc), preglomerular (P, PGa, PGl, PGm, and RT), and posterior tubercular (TPp and TPm) nuclei. Only scattered GAD67-expressing cells are seen in all pallial zones (Dm, Dd, Dc, Dl, and Dp) and in the previously unidentified bed nucleus of the stria medullaris (BNSM). The BNSM appears to be the adult teleostean derivative of the larval eminentia thalami (EmT). We identify the GAD67-positive entopeduncular nucleus proper (EN) as being homologous to the entopeduncular nucleus of nonprimate mammals. GAD67 is strongly expressed in the anterior thalamic nucleus (A). The anterior thalamic nucleus is laterally bordered by a distinct GAD67-expressing cell population, which we interpret as the previously unidentified reticular thalamic nucleus (RTN) of teleosts. Furthermore, we identified a GAD67-positive thalamic nucleus, the intercalated nucleus (IC), which is sandwiched between the GAD67-negative dorsal (DP) and central posterior (CP) thalamic nuclei. Overall, the distribution of GAD67-expressing cells highly resembles the distribution of gamma-aminobutyric acid (GABA)/GAD67-expressing cells found in the early zebrafish (teleost) forebrain and thus allows us to propose a prosomeric fate map of GABAergic cell populations.
Figures
Fig. 1
Distribution of _GAD67_-expressing cells in the zebrafish telencephalon (figs. A-E2). Note that _GAD67_-expressing cells in the (pallidal) entopeduncular nucleus (EN) are considerably larger compared to _GAD67_-expressing cells in the (septal) lateral nucleus of the area ventralis telencephali (Vl; fig. E1). For abbreviations, see list.
Fig. 2
Distribution of _GAD67_-expressing cells in the zebrafish telencephalon, preoptic region and habenula (A–D). Note the strip of _GAD67_-expressing cells (arrows in fig. A) reaching from a medial part of the area ventralis towards the entopeduncular nucleus (EN). For abbreviations, see list.
Fig. 3
Distribution of _GAD67_-expressing cells in the zebrafish diencephalon (A–D). Note migrated cells (white arrows) from the dorsal part of the periventricular pretectal nucleus (PPd) to the central pretectal nucleus (CPN) and other adjacent migrated pretectal nuclei such as the parvocellular superficial pretectal nucleus (PSp) and the magnocellular superficial pretectal nucleus (PSm). Also, note the arc of _GAD67_-expressing cells (black arrows) reaching from the boundary of the paraventricular organ (PVO of Rink and Wullimann, 2001) towards the periphery of the ventral zone of the periventricular hypothalamus (Hv). For abbreviations, see list.
Fig. 4
Distribution of _GAD67_-expressing cells in the preglomerular complex and hypothalamus (A–F). For abbreviations, see list.
Fig. 5
American tribal style schema of the adult zebrafish brain in sagittal view showing level of sections. Note that, for better understanding of _GAD67_-distribution, mid- and posterior hypothalamic level are shown in horizontal view.
Fig. 6
American tribal style schema of the adult zebrafish brain in sagittal view shows distribution of _GAD67_-expressing cells in the forebrain. Note that, for better understanding of _GAD67_-distribution, mid- and posterior hypothalamic level are shown in coronal perspective. The caudal hypothalamus (Hc) is free of _GAD67_-expressing cells but likely comprised of _GAD65_-expressing cells (indicated in grey) as shown in goldfish (Martyniuk et al., 2007). Black fields: heavily _GAD67_-labeled regions and nuclei. Black and white dots: scattered _GAD67_-expressing and _GAD67_-negative cells, respectively.
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References
- Abbott LC, Jacobowitz DM. Developmental expression of calretinin-immunoreactivity in the thalamic eminence of the fetal mouse. Int J Dev Neurosci. 1999;17:331–345. - PubMed
- Anglade I, Mazurais D, Douard V, Le Jossic-Corcos C, Mananos EL, Michel D, Kah O. Distribution of glutamic acid decarboxylase mRNA in the forebrain of the rainbow trout as studied by in situ hybridization. J Comp Neurol. 1999;410:277–289. - PubMed
- Barale E, Fasolo A, Girardi E, Artero C, Franzoni MF. Immunohistochemical investigation of gamma-aminobutyric acid ontogeny and transient expression in the central nervous system of Xenopus laevis tadpoles. J Comp Neurol. 1996;368:285–294. - PubMed
- Blader P, Fischer N, Gradwohl G, Guillemot F, Strähle U. The activity of neurogenin1 is controlled by local cues in the zebrafish embryo. Development. 1997;124:4557–4569. - PubMed
- Blader P, Plessy C, Strahle U. Multiple regulatory elements with spatially and temporally distinct activities control neurogenin1 expression in primary neurons of the zebrafish embryo. Mech Dev. 2003;120:211–218. - PubMed
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