Summary
In the present study, a temporal analysis of the pattern of distribution of serotoninergic fibers and varicosities within the cerebellum of pouch young opossums was carried out. Particular attention was focused on animals ranging in age from postnatal day (PD) 21-PD 72, because there is a transient expression of serotonin immunoreactivity in the cerebellar cortex during that interval. Between PD 1–33, there is a progressive increase in serotoninergic immunoreactivity throughout the cerebellar cortex. After PD 33, there is a decrease in the relative number of immunostained fibers followed by a reorganization into the adult pattern of distribution.
A double labeling paradigm, in which horseradish peroxidase, used as a retrograde marker, combined with serotonin immunohistochemistry was employed to localize serotoninergic neurons that project to the developing cerebellum. Initially (PD 9), serotoninergic cells in the medullary reticular formation and dorsolateral pontine tegmentum are double labeled. After PD 77, only neurons in the medullary reticular formation were double labeled.
The course taken by serotoninergic axons from the brainstem to the cerebellum also was analyzed. Between PD 1 and PD 42, serotoninergic axons enter the cerebellum via four different routes: 1) the inferior cerebellar peduncle; 2) a pathway located lateral and rostral to the inferior cerebellar peduncle; this bundle of serotonin axons contains immunoreactive fibers that also enter the tectum (this tract is referred to as the tecto-cerebellar bundle in this report); 3) the medial aspect of the superior cerebellar peduncle; and 4) the tela choroidea. After PD 40, the latter two pathways are the primary routes by which serotoninergic fibers enter the cerebellum. The loss of serotoninergic fibers in the first two pathways coincides with the decrease in serotoninergic immunoreactivity seen in the cerebellar cortex described above.
In summary, the results suggest that the serotoninergic projection to the opossum's cerebellum is remodelled during development. It is proposed that the serotonin fibers present at early stages of development may play a role in regulating specific events in cerebellar maturation. In contrast, the serotoninergic axons which have a more restricted pattern of distribution later in development, and in the adult, likely modulate neuronal activity within the cerebellum.
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Abbreviations
- BP :
-
basilar pons
- CB :
-
cerebellum
- CF :
-
cephalic flexure
- CN :
-
cerebellar nuclei
- CRI :
-
crus I
- CRII :
-
crus II
- DAO :
-
dorsal accessory olive
- DN :
-
dentate nucleus
- EGL :
-
external granule cell layer
- F :
-
flocculus
- FP :
-
primary fissue
- ICP :
-
interior cerebellar reduncle
- IO :
-
inferior olive
- IOC :
-
inferior olivary complex
- IV :
-
fourth ventricle
- LS :
-
lobus simplex
- MCP :
-
middle cerebellar peduncle
- MED :
-
medulla
- MID :
-
midbrain
- PF :
-
pontine flexure
- PFL :
-
paraflocculus
- PML :
-
paramedian lobule
- PN :
-
pontine nuclei
- PT :
-
pontine tegmentum
- RA :
-
raphe
- RGc v :
-
nucleus reticularis gigantocellularis pars ventralis
- SO :
-
superior olive
- SV :
-
superior medullary velum
- TC :
-
tela choroidea
- TE :
-
tectum
- VII :
-
facial nucleus
- Roman numerals I–X :
-
cerebellar lobules
References
Bishop GA, Ho RH (1985) The distribution and origin of serotonin immunoreactivity in the rat cerebellum. Brain Res 331:195–207
Bishop GA, Ho RH, King JS (1985a) An immunohistochemical study of serotonin development in the opossum cerebellum. Anat Embryol 171:325–338
Bishop GA, Ho RH, King JS (1985b) Localization of serotonin immunoreactivity in the opossum cerebellum. J Comp Neurol 235:301–321
Crutcher KA, Humbertson Jr AO (1978) The organization of monoamine neurons within the brainstem of the North American opossum (Didelphis virginiana). J Comp Neurol 179:195–222
Cutts JH, Krause WJ, Leeson CR (1978) General observations on the growth and development of the pouch young opossum. Biol Neonate 33:264–272
Holets V, Elde RP (1982) The differential distribution and relationships of serotonergic and peptidergic fibers of sympathoadrenal neurons in the intermediolateral cell column of the rat. A combined retrograde axonal transport and immunofluorescence study. Neuroscience 7:1155–1174
Holets V, Maley BE, Elde R (1981) Electron microscopic localization of 5-hydroxytryptamine immunoreactivity in the intermediolateral cell column of the cat. J Histochem Cytochem 28:890
King JS, Morgan J, Bishop GA, Hazlett JC, Martin GF (1987) Development of the basilar pons in the North American opossum: dendrogenesis and maturation of afferent and efferent connections. Anat Embryol 176:191–202
Lauder JM, Krebs H (1978) Serotonin as a differentiation signal in early neurogenesis. Dev Neuroscience 1:15–30
Lauder JM, Wallace JA, Krebs H, Petrusz P (1980) Serotonin as a timing mechanism in neuroembryogenesis. In: Brambilla F, Racagni G, DeWied D (eds) Progress in psychoneuroendocrinology, Elsevier/North Holland Biomedical Press Amsterdam, New York, pp 539–555
Laxson LC, King JS (1983) The formation and growth of the cortical layers in the cerebellum of the opossum. Anat Embryol 167:391–409
Martin GF, Cabana T, Humbertson AO (1982) The brainstem origin of monoaminergic projections to the spinal cord of the North American opossum: A study using fluorescent tracers and fluorescence histochemistry. Brain Res Bull 9:217–225
O'Donoghue DL, Martin GF, King JS (1987) The timing of granule cell differentiation and mossy fiber morphogenesis in the opossum. Anat Embryol 175:341–354
Sternberger LA (1979) Immunocytochemistry, Second Edition. John Wiley, New York
Strahlendorf JC, Hubbard DG (1983) Serotonergic interactions with rat cerebellar Purkinje cells. Brain Res Bull 11:265–269
Strahlendorf JC, Lee M, Strahlendorf HK (1984) Effects of serotonin on cerebellar Purkinje cells are dependent on the baseline firing rate. Exp Brain Res 56:50–58
Strahlendorf JC, Strahlendorf HK, Lee M (1986) Enhancement of cerebellar Purkinje cell complex discharge activity by microiontophoretic serotonin. Exp Brain Res 61:614–624
Walker JJ, Bishop GA, Ho RH, King JS (1986) The brainstem origin of serotoninergic and enkephalinergic projections to the opossum's cerebellum. Anat Rec 214:139A
Walker JJ, Bishop GA, Ho RH, King JS (1988) The brainstem origin of serotonin and enkephalin immunoreactive afferents to the opossum's cerebellum. J Comp Neurol, in press
Yew DT, Ho AKS, Meyer DB (1974) Effect of 6-hydroxydopamine on retinal development in the chick. Experentia 30:1320–1322
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Bishop, G.A., Ho, R.H. & King, J.S. A temporal analysis of the origin and distribution of serotoninergic afferents in the cerebellum of pouch young opossums. Anat Embryol 179, 33–48 (1988). https://doi.org/10.1007/BF00305098
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DOI: https://doi.org/10.1007/BF00305098