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vglut2 and gad expression reveal distinct patterns of dual GABAergic versus glutamatergic cotransmitter phenotypes of dopaminergic and noradrenergic neurons in the zebrafish brain.

Filippi A, Mueller T, Driever W - J. Comp. Neurol. (2014)

Bottom Line: Our results show that most dopaminergic neurons also express GABAergic markers, including the dopaminergic groups of the olfactory bulb (homologous to mammalian A16) and the subpallium, the hypothalamic groups (A12, A14), the prethalamic zona incerta group (A13), the preoptic groups (A15), and the pretectal group.All together, our results demonstrate that all catecholaminergic groups in zebrafish are either GABAergic or glutamatergic.We compare our results with those that have been described for mammalian systems, discuss the phenomenon of transmitter dualism in the context of developmental specification of GABAergic and glutamatergic regions in the brain, and put this phenomenon in an evolutionary perspective.

View Article: PubMed Central - PubMed

Affiliation: Developmental Biology, Institute of Biology I, Faculty of Biology, Albert-Ludwigs-University Freiburg, 79104, Freiburg, Germany.

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Expression of the glutamatergic marker vglut2 in relation to TH immunoreactivity at 96 hpf. A: Schematic lateral (top) and dorsal (bottom) views of the zebrafish larval brain showing the distribution of catecholaminergic groups detectable by immunohistochemistry at 4 dpf (modified from Tay et al., 2011). B1,B2: overviews indicating planes of histological sections (for details, see Fig. 1B1,B2). C–J: Fluorescent in situ hybridization to vglut2 (green) combined with anti-TH immunofluorescence (red). Left panels (C–J) show overviews of dorsal views for planes encompassing different TH-ir clusters. Right panels (D1–D3 through J2) show enlargements of the areas framed by white boxes in the overviews. The only groups that appear to express vglut2 are the Otp-dependent groups 2,4–6 in the posterior tuberculum/hypothalamus (E,E2, G,G2). The pretectal group (C), the prethalamic group 1 (E,E2), the hypothalamic groups 3 and 7 (G,G2, I,I2), and the preoptic group (J,J2) do not express vglut2. The noradrenergic neurons of the locus coeruleus (D–D3) are intermingled with vglut2-expressing cells, but they do not appear to express vglut2. The telencephalic groups in the olfactory bulb and in the subpallium (F,F2 and H,H2, respectively) do not express vglut2 but are located in areas adjacent to vglut2-expressing neurons. All images in C–J are 4–13-μm confocal z-projections, except for those in D1–D3, which show a single confocal plane. For abbreviations, see list. A magenta–green copy of this figure is available as Supporting Information Figure S2. Scale bar = 50 μm in B1 (applies to B1,B2), C, D, D3 (applies to D1–D3), E, E2 (applies to E1,E2), F, G, G2 (applies to G1,G2), I, I2 (applies to I2,I2), J.
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fig02: Expression of the glutamatergic marker vglut2 in relation to TH immunoreactivity at 96 hpf. A: Schematic lateral (top) and dorsal (bottom) views of the zebrafish larval brain showing the distribution of catecholaminergic groups detectable by immunohistochemistry at 4 dpf (modified from Tay et al., 2011). B1,B2: overviews indicating planes of histological sections (for details, see Fig. 1B1,B2). C–J: Fluorescent in situ hybridization to vglut2 (green) combined with anti-TH immunofluorescence (red). Left panels (C–J) show overviews of dorsal views for planes encompassing different TH-ir clusters. Right panels (D1–D3 through J2) show enlargements of the areas framed by white boxes in the overviews. The only groups that appear to express vglut2 are the Otp-dependent groups 2,4–6 in the posterior tuberculum/hypothalamus (E,E2, G,G2). The pretectal group (C), the prethalamic group 1 (E,E2), the hypothalamic groups 3 and 7 (G,G2, I,I2), and the preoptic group (J,J2) do not express vglut2. The noradrenergic neurons of the locus coeruleus (D–D3) are intermingled with vglut2-expressing cells, but they do not appear to express vglut2. The telencephalic groups in the olfactory bulb and in the subpallium (F,F2 and H,H2, respectively) do not express vglut2 but are located in areas adjacent to vglut2-expressing neurons. All images in C–J are 4–13-μm confocal z-projections, except for those in D1–D3, which show a single confocal plane. For abbreviations, see list. A magenta–green copy of this figure is available as Supporting Information Figure S2. Scale bar = 50 μm in B1 (applies to B1,B2), C, D, D3 (applies to D1–D3), E, E2 (applies to E1,E2), F, G, G2 (applies to G1,G2), I, I2 (applies to I2,I2), J.

Mentions: gad1b and gad2 expression has been shown to largely overlap in the developing brain of several model organisms (Ahman et al., 1996; Dupuy and Houser, 1996; Martin et al., 1998). Indeed, a gross comparison of their expression patterns by FISH showed that they are both expressed in a similar manner in major areas of the zebrafish brain at 4 dpf (data not shown). We focused our analysis on the potential colocalization of gad1b/2 with TH immunoreactivity in larval DA clusters, and detected some differences in the distribution of gad1b/2 transcripts in specific nuclei of the brain. Our results are shown in Figure 1, organized from dorsal to ventral (see Fig. 1A, B1, B2 for orientation on the distribution of TH-immunoreactive clusters), and summarized in Table2.


vglut2 and gad expression reveal distinct patterns of dual GABAergic versus glutamatergic cotransmitter phenotypes of dopaminergic and noradrenergic neurons in the zebrafish brain.

Filippi A, Mueller T, Driever W - J. Comp. Neurol. (2014)

Expression of the glutamatergic marker vglut2 in relation to TH immunoreactivity at 96 hpf. A: Schematic lateral (top) and dorsal (bottom) views of the zebrafish larval brain showing the distribution of catecholaminergic groups detectable by immunohistochemistry at 4 dpf (modified from Tay et al., 2011). B1,B2: overviews indicating planes of histological sections (for details, see Fig. 1B1,B2). C–J: Fluorescent in situ hybridization to vglut2 (green) combined with anti-TH immunofluorescence (red). Left panels (C–J) show overviews of dorsal views for planes encompassing different TH-ir clusters. Right panels (D1–D3 through J2) show enlargements of the areas framed by white boxes in the overviews. The only groups that appear to express vglut2 are the Otp-dependent groups 2,4–6 in the posterior tuberculum/hypothalamus (E,E2, G,G2). The pretectal group (C), the prethalamic group 1 (E,E2), the hypothalamic groups 3 and 7 (G,G2, I,I2), and the preoptic group (J,J2) do not express vglut2. The noradrenergic neurons of the locus coeruleus (D–D3) are intermingled with vglut2-expressing cells, but they do not appear to express vglut2. The telencephalic groups in the olfactory bulb and in the subpallium (F,F2 and H,H2, respectively) do not express vglut2 but are located in areas adjacent to vglut2-expressing neurons. All images in C–J are 4–13-μm confocal z-projections, except for those in D1–D3, which show a single confocal plane. For abbreviations, see list. A magenta–green copy of this figure is available as Supporting Information Figure S2. Scale bar = 50 μm in B1 (applies to B1,B2), C, D, D3 (applies to D1–D3), E, E2 (applies to E1,E2), F, G, G2 (applies to G1,G2), I, I2 (applies to I2,I2), J.
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fig02: Expression of the glutamatergic marker vglut2 in relation to TH immunoreactivity at 96 hpf. A: Schematic lateral (top) and dorsal (bottom) views of the zebrafish larval brain showing the distribution of catecholaminergic groups detectable by immunohistochemistry at 4 dpf (modified from Tay et al., 2011). B1,B2: overviews indicating planes of histological sections (for details, see Fig. 1B1,B2). C–J: Fluorescent in situ hybridization to vglut2 (green) combined with anti-TH immunofluorescence (red). Left panels (C–J) show overviews of dorsal views for planes encompassing different TH-ir clusters. Right panels (D1–D3 through J2) show enlargements of the areas framed by white boxes in the overviews. The only groups that appear to express vglut2 are the Otp-dependent groups 2,4–6 in the posterior tuberculum/hypothalamus (E,E2, G,G2). The pretectal group (C), the prethalamic group 1 (E,E2), the hypothalamic groups 3 and 7 (G,G2, I,I2), and the preoptic group (J,J2) do not express vglut2. The noradrenergic neurons of the locus coeruleus (D–D3) are intermingled with vglut2-expressing cells, but they do not appear to express vglut2. The telencephalic groups in the olfactory bulb and in the subpallium (F,F2 and H,H2, respectively) do not express vglut2 but are located in areas adjacent to vglut2-expressing neurons. All images in C–J are 4–13-μm confocal z-projections, except for those in D1–D3, which show a single confocal plane. For abbreviations, see list. A magenta–green copy of this figure is available as Supporting Information Figure S2. Scale bar = 50 μm in B1 (applies to B1,B2), C, D, D3 (applies to D1–D3), E, E2 (applies to E1,E2), F, G, G2 (applies to G1,G2), I, I2 (applies to I2,I2), J.
Mentions: gad1b and gad2 expression has been shown to largely overlap in the developing brain of several model organisms (Ahman et al., 1996; Dupuy and Houser, 1996; Martin et al., 1998). Indeed, a gross comparison of their expression patterns by FISH showed that they are both expressed in a similar manner in major areas of the zebrafish brain at 4 dpf (data not shown). We focused our analysis on the potential colocalization of gad1b/2 with TH immunoreactivity in larval DA clusters, and detected some differences in the distribution of gad1b/2 transcripts in specific nuclei of the brain. Our results are shown in Figure 1, organized from dorsal to ventral (see Fig. 1A, B1, B2 for orientation on the distribution of TH-immunoreactive clusters), and summarized in Table2.

Bottom Line: Our results show that most dopaminergic neurons also express GABAergic markers, including the dopaminergic groups of the olfactory bulb (homologous to mammalian A16) and the subpallium, the hypothalamic groups (A12, A14), the prethalamic zona incerta group (A13), the preoptic groups (A15), and the pretectal group.All together, our results demonstrate that all catecholaminergic groups in zebrafish are either GABAergic or glutamatergic.We compare our results with those that have been described for mammalian systems, discuss the phenomenon of transmitter dualism in the context of developmental specification of GABAergic and glutamatergic regions in the brain, and put this phenomenon in an evolutionary perspective.

View Article: PubMed Central - PubMed

Affiliation: Developmental Biology, Institute of Biology I, Faculty of Biology, Albert-Ludwigs-University Freiburg, 79104, Freiburg, Germany.

Show MeSH
Related in: MedlinePlus