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The process of background adaptation in the toad Xenopus laevis is controlled by neurons in the suprachiasmatic nucleus (SC) that inhibit the release of alpha-melanophore-stimulating hormone from the neuroendocrine melanotrope cells in the pituitary gland. We have identified the structural and functional organization of different neuropeptide Y (NPY)-containing cell groups in the Xenopus SC in relation to background adaptation. A ventrolateral, a dorsomedial, and a caudal group were distinguished, differing in location as well as in number, size, and shape of their cells. They also show different degrees of NPY immunoreactivity in response to different background adaptation conditions. In situ hybridization using a Xenopus mRNA probe for the exocytosis protein DOC2 revealed that melanotrope cells of black-adapted animals have a much higher expression of DOC2-mRNA than white-adapted ones. This establishes that the degree of DOC2-mRNA expression is a good parameter to measure cellular secretory activity in Xenopus. We show that in the ventrolateral SC group, more NPY-positive neurons express DOC2-mRNA in white- than in black-adapted animals. In contrast, NPY-positive neurons in the dorsomedial group have a high secretory activity under the black-adaptation condition. We propose that in black-adapted animals, NPY-positive neurons in the ventrolateral group, known to inhibit the melanotrope cells in white-adapted animals synaptically, are inhibited by NPY-containing interneurons in the dorsmedial group. NPY-positive neurons in the caudal group have similar secretory dynamics as the dorsomedial NPY neurons, indicating that they also play a role in background adaptation, distinct from that exerted by the ventrolateral and dorsomedial group.
Fig. 2. Diameters of cell body profiles in the ventrolateral (VL),
dorsomedial (DM), and caudal (C) group of the SC. Values are expressed
as means 6 SEM. Bars with a different superscript differ
significantly (P , 0.05).
Fig. 3. NPY-immunoreactive neurons in (A) the ventrolateral (VL) and dorsomedial (DM) and (B) the
caudal group of the SC. Arrows indicate axons projecting from cells in the dorsomedial group toward the
ventrolateral group. C: Detail of cell in the ventrolateral group. Asterisks indicate NPY-positive varicosities
in close contact with the cell. Scale bars 5 15 mm in A and B; 6.5 mm in C.
Fig. 4. In situ hybridization of DOC2-mRNA in (A) the ventrolateral (VL) and dorsomedial (DM) and
(B) the caudal (C) group of the SC. No signal is present when the sense mRNA probe is used (C). OC, optic
chiasm; III, third ventricle. Scale bar 5 100 mm.
Fig. 5. Immunofluorescence of NPY (A,B) and in situ hybridization of DOC2 mRNA (C,D) in the
pituitary of white- (A, C) and black- (B, D) adapted Xenopus laevis. pd, pars distalis; pi, pars intermedia;
pn, pars nervosa. Scale bar 5 75 mm.
Fig. 6. Optical density (O.D.) of DOC2-mRNA hybridization signal
in the pars intermedia of white- (W), gray- (G), and black- (B) adapted
animals. Values are expressed in arbitrary units (a.u.) as means 6
SEM. Bars with a different superscript differ significantly (P , 0.05).
Fig. 7. Immunofluorescence of NPY (A,C,E) and in situ hybridization
of DOC2-mRNA (B,D,F) in the dorsomedial (A,B), ventrolateral
(C,D), and caudal (E,F) cell groups of the SC. Asterisks indicate
coexistence of DOC2-mRNA and NPY peptide in the same neuron.
Arrows indicate neurons positive for NPY but negative for DOC2-
mRNA. Note that many neurons are positive for DOC2-mRNA but
negative for NPY. Scale bar 5 13 mm.
Fig. 8. Number of NPY-immunoreactive cell profiles per section
(A), staining intensity of NPY-immunoreactive profiles (B), and number
of NPY-immunoreactive profiles positive for DOC2-mRNA per
section (C), in the ventrolateral (VL), dorsomedial (DM), and caudal
(C) cell group of the SC, in white- (W), gray- (G), and black- (B)
adapted animals. Values are expressed as means 6 SEM. Bars with a
different superscript differ significantly (P , 0.05).
Fig. 9. Number of NPY-immunoreactive cell profiles (A) and number
of NPY-immunoreactive cell profiles positive for DOC2-mRNA (B),
per section, in the ventromedial thalamic nucleus of white- (W) and
black- (B) adapted animals. Values are expressed as means 6 SEM.
The groups do not differ statistically.
Fig. 10. Schematic representation of the hypothesized role of the
three NPY-immunoreactive neuronal cell groups in the SC of Xenopus
laevis, representing a sagittal section through the brain. All neuronal
projections shown are inhibitory. For the caudal group, multiple functional
roles are hypothesized (see text), of which only one is depicted
in this figure. a-MSH, a-melanophore-stimulating hormone; C, caudal
group, DM, dorsomedial group; PI, pars intermedia; VL, ventrolateral
group.
