Summary
Calbindin D-28k immunoreactivity appeared at embryonal day 14 (E14) in the central nervous system as well as in the sensory organs and at E15 in the peripheral nervous system of the rat. At E14 the infundibular process of the diencephalon, cells of the posterior hypothalamus and of the dorsal thalamus were the only structures strongly immunostained in the brain, whereas neurons of the basal plate of the spinal cord, medulla oblongata and of the out-ermost layer of the cerebral cortex were only faintly labeled. Calbindin positive cerebellar Purkinje cells could be discerned at E15 together with a few cells in the hippocampus and in ganglia of the cranial nerves. At E19 various mesencephalic and metencephalic structures, spinal ganglion cells and basal ganglia displayed calbindin immunoreactive cells. The adult pattern of calbindin immunoreactivity (Garcia Segura et al. 1984) was reached before birth in most brain regions. In general, cells which displayed calbindin during brain development were also calbindin positive in the adult animal. Exceptions to this rule were cells of the deep nuclei of the cerebellum and non-neuronal cells which transiently expressed calbindin during development. Calbindin appeared in a given brain region almost invariably 1 or 2 days after the cessation of cell division and the beginning of neuronal migration and extension of neuronal processes. The calcium binding protein calbindin might influence these Ca2+-dependent processes.
Similar content being viewed by others
Abbreviations
- A :
-
Axon
- ac :
-
anterior commissure
- Acq :
-
Aqueductus cerebri
- AH :
-
Adenohypophysis
- AMY :
-
Amygdala
- aV :
-
anterior vermis
- BG :
-
Basal Ganglia
- BO :
-
Bulbus olfactorius
- BPG :
-
basal pontine grey
- C :
-
Cortex
- CA :
-
Crista ampullaris
- cer :
-
Cerebellum
- CO :
-
otic cyst
- CP :
-
choroid plexus
- CPT :
-
Caudatoputamen
- DCN :
-
deep cerebellar nuclei
- DT :
-
dorsal thalamus
- E :
-
foregut epithelium
- ec :
-
external capsule
- eml :
-
external medullary lamina
- ENP :
-
entopeduncular nucleus
- EP :
-
Ependym
- ET :
-
Epithalamus
- EY :
-
eye
- F :
-
Fimbria
- fo :
-
Fornix
- fr :
-
Fasciculus retroflexus
- GP :
-
Globus pallidus
- gr :
-
granular laver of the cerebellum
- Gsp :
-
ganglion spirale cochlea
- HI :
-
Hippocampus
- HYP :
-
Hypothalamus
- I :
-
hippocampal interneurons
- ic :
-
internal capsule
- IE :
-
inner ear
- IH :
-
inner hair cells of the cochlea
- IO :
-
inferior olive
- IS :
-
internal sulcus cells of the cochlea
- LD :
-
laterodorsal thalamus
- LV :
-
lateral ventricle
- MB :
-
mamillary body
- MH :
-
medial habenular nucleus
- mol :
-
molecular layer of the cerebellum
- mt :
-
mamillo-thalamic tract
- mtt :
-
mamillo-tegmental tract
- N :
-
nose
- n :
-
olfactory nerve
- NBM :
-
Nucleus basalis of Meynert
- NE :
-
nose epithelium
- NH :
-
Neurohypophysis
- NRT:
-
Nucleus reticularis tegmenti pontis
- ON :
-
olfactory nuclei
- OR :
-
optic recess
- PC :
-
posterior commissure
- PG :
-
Epiphysis
- PI :
-
inferior cerebellar peduncle
- PS :
-
superior cerebellar peduncle
- PU :
-
Purkinje cell
- PV :
-
paraventricular hypothalamic nucleus
- pV :
-
posterior vermis
- PVP :
-
paraventricular thalamic nucleus
- PY :
-
pyramidal cells of the hippocampus
- RA :
-
Raphe nuclei
- RE :
-
Nucleus reuniens
- RH :
-
Nucleus rhomboideus
- RN :
-
reticular nucleus
- RP :
-
Rathke's pouch
- sc :
-
spinal cord
- SG :
-
substantia gelatinosa Rolandi
- slm :
-
Stratum-lacunosum molecular
- sm :
-
Stria medullaris
- SN :
-
Substantia nigra
- SO :
-
supraoptic nucleus
- Sol :
-
Nucleus of the solitary tract
- Tect :
-
Tectum
- Teg :
-
Tegmentum
- TG :
-
tegmental nucleus of Gudden
- Tg :
-
tongue
- TO :
-
tuberculum olfactorium
- VT :
-
ventral thalamus
- WH :
-
white matter
- ZI :
-
Zona incerta
- 3 :
-
third ventricle
- 4 :
-
fourth ventricle
- II N :
-
Nervus opticus
- Vg :
-
Trigeminal ganglion
- Vsp :
-
spinal trigeminal nucleus
- VIIG :
-
Ganglion geniculi
- VIIIG :
-
Ganglion vestibulare
- IXGI :
-
interior ganglion of IX
- IXGS :
-
superior ganglion of IX
- XGI :
-
inferior ganglion of X
References
Altman J (1972b) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of molecular layer. J Comp Neurol 145:399–464
Altman J, Bayer SA (1978a) Development of the diencephalon in the rat. I. Autoradiographic study of the time of origin and settling patterns of neurons of the hypothalamus. J Comp Neurol 182:945–972
Altman J, Bayer SA (1978b) Prenatal development of the cerebellar system in the rat. J Comp Neurol 179:23–48
Altman J, Bayer SA (1978c) Development of the diencephalon in the rat. III. Ontogeny of the specialized ventricular lining of the hypothalamic third ventricle. J Comp Neurol 182:995–1016
Altman J, Bayer SA (1979) Development of the diencephalon in the rat. V: Thymidine radiographic observation on internuclear gradients in the thalamus. J Comp Neurol 188:473–500
Altman J, Bayer SA (1980a) Development of the brainstem in the rat. I. Thymidine-radiographic study of the time of origin of neurons of the lower medulla. J Comp Neurol 194:1–36
Altman J, Bayer SA (1980b) Development of the brain stem in the rat II. A Thymidine radiographic study of the time of origin of neurons of the upper medulla, excluding the vestibular and auditory nuclei. J Comp Neurol 194:37–65
Altman J, Bayer SA (1980c) Development of the brain stem in the rat. III. Thymidine radioautographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla. J Comp Neurol 194:877–904
Altman J, Bayer SA (1981) The time of origin of neurons of the rat superior colliculus in relation to other components of the visual and visuomotor pathways. Exp Brain Res 42:424–434
Altman J, Bayer SA (1982) Development of the cranial nerve ganglion and related nuclei in the rat. Adv Anat Embryol Cell Biol 74:1–90
Altman J, Bayer SA (1984) Development of the spinal cord. Adv Anat Embryol Cell Biol 85:1–164
Baimbridge KG, Miller JJ (1982) Immunohistochemical localization of calcium binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res 245:223–229
Bayer SA (1979) The development of the septal region in the rat. I. neurogenesis examined with Thymidine autoradiography. J Comp Neurol 183:89–106
Bayer SA (1980a) Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-Thymidine autoradiography. J Comp Neurol 190:87–114
Bayer SA (1980b) Quantitative 3H-thymidine radioautographic analysis of neurogenesis in the rat amygdala. J Comp Neurol 194:845–875
Bayer SA (1983) 3H-Thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res 50:329–340
Bishop JE, Norman AW (1975) Metabolism of 25-hydroxy-vitamin D3 in the chick embryo. Arch Biochem Biophys 167:769–773
Campbell AK (1983) Intracellular calcium. Wiley and Son, Chichester
Celio MR (1984) Calcium binding proteins in the rat brain. Habilitationsschrift Universität Zürich, pp 1–100
Celio MR, Norman AW (1985) Nucleus basalis Meynert neurons contain the vitamin D-dependent calcium binding protein (calbindin D-28k). Anat Embryol 173:143–148
Cheung EJ (1980) Calmodulin plays a pivotal role in cellular regulation. Science 207:19–27
Christakos S, Friedlander EJ, Frandsen BR, Norman AW (1979) Studies on the mode of action of calciferol. XII. Development of a radioimmunoassay for calbindin D-28k. Endocrinol 104:1495–1503
Garcia-Segura LM, Baetens D, Roth J, Norman AW, Orci L (1984) Immunohistochemical mapping of calcium binding protein in the rat central nervous system. Brain Res 296:75–86
Ito M (1984) The cerebellum. Raven press
Iurato S (1962) Functional implications of the nature and submicroscopic structure of the tectorial and basilar membrane. J Acoust Soc Am 34:1386–1395
Iurato S (1967) Submicroscopic structure of the inner ear. Pergamon press
Jande SS, Maler L, Lawson DEM (1981) Immunohistochemical mapping of Vitamin D-dependent calcium binding protein in brain. Nature 294:765–767
Kazazoglou T, Schmid A, Renaud JF, Ladzunski M (1983) Ontogenetic appearance of Ca2+ channels characterized as binding sites for nitrendipine during development of nervous, skeletal and cardiac muscle systems in the rat. FEBS Lett 164:75–79
König N, Roch G, Marty R (1975) The onset of synaptogenesis in rat temporal cortex. Anat Embryol 148:73–87
König N, Mathys R (1981) Early neurogenesis and synaptogenesis in the cerebral cortex. Bibliotheca anatomica 19:152–160
Legrand Ch, Thomasset M, Parkes CO, Clavel MC, Rabié A (1983) Calcium binding protein in the developing rat cerebellum. Cell Tissue Res 233:389–402
Lidov HGW, Molliver ME (1982) Immunohistochemical study of the development of serotonergic neurons in the rat CNS. Brain Res Bull 9:559–604
Lim DJ (1977) Fine morphology of the tectorial membrane (fresh and developmental). In: Inner ear Biology. Portman M, Aran JM (eds) INSERM 18, pp 47–60
Marchand R, Lajoie L (1986) Histogenesis of the strio-pallidal system in the rat. Neurogenesis of its neurons. Neuroscience 17:573–590
Marin-Padilla M (1984) Neurons of layer I. A developmental Analysis. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Plenum Press New York, 1985
Rabié A, Thomasset M, Legrand Ch (1983) Immunocytochemical detection of calcium-binding protein in the cochlear and vestibular hair cells of the rat. Cell Tissue Res 232:691–696
Raedler R, Raedler A (1978) Autoradiographic study of early neurogenesis in rat neocortex. Anat Embryol 154:267–284
Roth J, Baetens D, Norman AW, Garcia Segura LM (1981) Specific neurons in the chick central nervous system stain with an antibody against chicken intestinal Vitamin D-dependent calcium binding protein. Brain Res 222:452–457
Ruben RJ (1967) Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol [Suppl] 220:1–44
Schneeberger PR, Norman AW, Heizmann CW (1985) Neurosci Lett 59:97–103
Straus W (1976) Use of peroxydase inhibitors for immunoperoxydase methods. In: Immunoenzymatic techniques. INSERM. Elsevier, pp 117–125
Wallace JA, Lauder JM (1983) Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res Bull 10:459–479
Wassermann RH, Taylor AN (1966) Vitamin D-induced calcium binding protein in chick intestinal mucosa. Science 152:791–793
Wassermann RH, Fullmer CS (1982) Vitamin D induced calcium binding protein. In: Cheung ED (ed) Calcium and cell function, vol II. Academic press
Wassermann RH (1985) Nomenclature of the Vitamin D-induced calcium binding protein. In: Norman AW, Schaefer K, Grigoilet HG, Herrath D v (eds) Vitamin D. Walter de Gruyter Berlin New York, pp 321–323
Weibel ER (1957) Zur Kenntnis der Differenzierungsvorgänge im Epithel des Ductus Cochlearis. Acta Anat 29:53–90
Author information
Authors and Affiliations
Additional information
Submitted by S.E. as her doctoral thesis at the medical faculty of the University of Zürich
Rights and permissions
About this article
Cite this article
Enderlin, S., Norman, A.W. & Celio, M.R. Ontogeny of the calcium binding protein calbindin D-28k in the rat nervous system. Anat Embryol 177, 15–28 (1987). https://doi.org/10.1007/BF00325286
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00325286