Summary
In the adult rat brain, the calcium-binding protein parvalbumin is preferentially associated with spontaneously fast-firing, metabolically active neurons and coexists with gamma-amino-butyric acid (GABA) in cortical inhibitory interneurons. Whether this is so in developing neurons has not been explored. To this end, we have used parvalbumin immunohistochemistry to study expression of this protein in the rat nervous system during pre- and postnatal life. Our results indicate that parvalbumin first appears at embryonic day 13 in sensory system of the spinal cord, in the vestibular (VIII), the trigeminal (V) and the visuomotor (III, IV VI) systems, and develops rapidly during the following days. In these locations the expression of parvalbumin coincides with the beginning of physiological activity in nerve cells. In the gamma-aminobutyric acid (GABA)-containing interneurons of the cerebral cortex and the hippocampus, as well as in the Purkinje cells of the cerebellum, parvalbumin only appears postnatally. It lags behind the development of GABA-immunoreactivity by 1 to 2 weeks. The beginning of its expression, in the cerebellum at least, coincides with the arrival of excitatory synaptic input and the onset of spontaneous activity. Thus, during the development of the nervous system, the expression of parvalbumin is subordinate to the establishment of physiological activity.
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Abbreviations
- 3:
-
oculomotor nucleus
- 4:
-
trochlear nucleus
- 4n:
-
trochlear nerve
- 6:
-
abducens nucleus
- 12:
-
hypoglossal nucleus
- 3n:
-
oculomotor nerve
- 4V:
-
4th ventricle
- 5g:
-
trigeminal ganglion
- 5n:
-
trigeminal nerve
- 5mx:
-
trigeminal nerve, maxillary branch
- 8c1:
-
cochlear ganglion
- 8g:
-
vestibular ganglion
- 8n:
-
vestibular nerve
- 10n:
-
vagal nerve
- Amb:
-
ambiguus nucleus
- CaBP:
-
calcium-binding protein
- Ce:
-
cerebellum
- ChP:
-
choroid plexus
- cl:
-
cochlea
- CPu:
-
caudate putamen
- Cu:
-
cuneate nucleus
- Cx:
-
cerebral cortex
- df:
-
dorsal funiculus spinal cord
- dr:
-
dorsal root spinal nerve
- E15:
-
embryonic day 15 of gestation
- ECN:
-
external cuneate nucleus
- Fr:
-
formatio reticularis
- GABA:
-
gamma-amino-butyric acid
- GAD:
-
glutamate decarboxylase
- gl:
-
granular layer cerebellum
- Gr:
-
gracile nucleus
- Hip:
-
hippocampus
- H:
-
heart
- inc:
-
inferior colliculus
- IOK:
-
inferior olive, kap cooy medial nucleus
- Li:
-
liver
- LMol:
-
lacunosum moleculare layer hippocampus
- Lu:
-
lung
- LV:
-
lateral ventricle
- LVe(v):
-
lateral vestibular nucleus (ventral)
- LVe(d):
-
lateral vestibular nucleus (dorsal)
- me5:
-
mesencephalic trigeminal tract
- Me5:
-
mesencephalic trigeminal nucleus
- Mes:
-
mesencephalon
- ml:
-
molecular layer cerebellum
- MVe:
-
medial vestibular nucleus
- Or:
-
oriens layer hippocampus
- P 2:
-
postnatal day 2
- Pu:
-
Purkinje-cell layer, cerebellum
- Py:
-
pyramidal cell layer, hippocampus
- R:
-
red nucleus
- Rhom:
-
rhombencephalon
- Rt:
-
reticular thalamic nucleus
- sk:
-
skin
- sn:
-
substantia nigra
- spgl:
-
spinal ganglion
- sp5:
-
spinal trigeminal tract
- SpVe:
-
spinal vestibular nucleus
- Sp5I:
-
spinal trigeminal nucleus, interpolar
- suc:
-
superior colliculus
- SuVe:
-
superior vestibular nucleus
- TBS:
-
tris-buffered saline
- tch:
-
tactile hair sinus
- ve:
-
vestibular epithelium
- vb:
-
vertebral body
- vh:
-
ventral horn spinal cord
- VL:
-
ventrolateral thalamic nucleus
- VP:
-
ventral pallidum
- vr:
-
ventral root spinal nerve
References
Altman J (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and the molecular layer. J Comp Neurol 145:399–464
Altman J, Bayer SA (1979) Development of the diencephalon of the rat. V. Thymidine-radiographic observations on internuclear and intranuclear gradients in the thalamus. J Comp Neurol 188:473–500
Altman J, Bayer SA (1980a) Development of the brain stem in the rat. II. Thymidine-radiographic study of the time of origin of neurons of the upper medulla, excluding the vestibular and auditory nuclei. J Comp Neurol 194:37–56
Altman J, Bayer SA (1980b) Development of the brain stem of the rat. 111. Thymidine-radiographic 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 (1981a) Development of the brain stem in the rat. V. Thymidine-radiographic study of the time of origin of neurons in the midbrain tegmentum. J Comp Neurol 198:677–716
Altman J, Bayer SA (1981b) 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 ganglions and related nuclei in the rat. Adv Anat Embryol Cell Biol 74:1–90
Altman J, Bayer SA (1985) Embryonic development of the rat cerebellum. III. Regional differences in the time of origin, migration and settling of Purkinje cells. J Comp Neurol 231:42–65
Amaral DG, Kurz J (1985) The time of origin of cells demonstrating glutamic acid decarboxylase-like immunoreactivity in the hippocampal formation of the rat. Neurosci Lett 59:33–39
van Bartheld SC, Rubel EW (1989) Transient GABA-immunoreactivity in cranial nerves of the chick embryo. J Comp Neurol 286:456–471
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) Development of the hippocampal regions in the rat. 11. Morphogenesis during embryonic and early postnatal life. J Comp Neurol 190:115–134
Berchtold MW, Celio MR, Heizmann CW (1984) Parvalbumin in non-muscle tissues of the rat. J Biol Chem 259:5189–5196
Berry M, Rogers W (1965) The migration of neuroblasts in the developing cerebral cortex. J Anat 99:691–709
Bieger D, Hopkins DA (1987) Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol 262:546–562
Bourne JA (1983) Handbook of immunoperoxidase staining methods. DAKO corporation. Santa Barbara, Calif. 93103
Braun K, Scheich H, Schachner M, Heizmann CW (1985) Distribution of parvalbumin, cytochrome oxidase activity and 14C-2-deoxyglucose uptake in the brain of the zebra finch. II. Visual system. Cell Tissue Res 240:117–127
Celio MR (1984) Parvalbumin as a marker of fast firing neurons. Neurosci Lett [Suppl 18]:322
Celio MR (1987) Parvalbumin in most gamma-amino-butyric acid-containing neurons of the rat cerebral cortex. Science 231:995–997
Celio MR (1989) Calcium-binding proteins in the brain. Arch Ital Anat Embriol 94:227–236
Celio MR (1970) Calcium-binding proteins in the rat nervous system. Neuroscience 35:375–475
Celio MR, Heizmann CW (1981) Calcium-binding protein parvalbumin as a neuronal marker. Nature 293:300–302
Celio MR, Baier W, Schäfer L, de Viragh PA, Gerday CH (1988) Monoclonal antibodies directed against the calcium-binding protein parvalbumin. Cell Calcium 9:81–86
Cheung EJ (1980) Calmodulin plays a pivotal role in cellular regulation. Science 207:19–27
Chromwall BM, Wolff JR (1980) Prenatal and postnatal development of GABA-accumulating cells in the occipital cortex of the rat. J Comp Neurol 190:187–208
Chung K, Coggeshall RE (1987) Postnatal development of the rat dorsal funiculus. J Neurosci 7:972–977
Clarke PGH (1989) Development cell death: morphological diversity and multiple mechanisms. Anat Embryol 263:1–19
Dennis MJ, Ziskind-Conhaim L, Harris AJ (1981) Development of neuromuscular junctions in rat embryos. Dev Biol 81:266–279
Deuticke HJ (1934) Über die Sedimentationskonstante von Muskelproteinen. Hoppe-Seyler's Z Physiol Chem 224:216–238
van Eden CG, Mrzijak L, Voorn P, Uyilings HBM (1989) Prenatal development of GABA-ergic neurons in the neocortex of the rat. J Comp Neurol 289:213–227
Enderlin S, Norman AW, Celio MR (1987) Ontogeny of the calcium-binding protein calbindin D-28k in the rat nervous system. Anat Embryol 177:15–28
Endo T, Ashi SK, Onaya T (1985) Parvalbumin in rat cerebrum, cerebellum and retina during postnatal development. Neurosci Lett 60:279–282
Fitzgerald M (1985) The post-natal development of cutaneous afferent fibre input and receptive field organisation in the rat dorsal horn. J Physiol 364:1–18
Fitzgerald M (1997) Cutaneous primary afferent properties in the hindlimb of the neonatal rat. J Physiol 383:79–92
Foster GA, Schultzberg M, Goldstein M, Hökfelt T (1985) Ontogeny of phenylthanolamine N-methyltransferase- and tyrosine hydroxylase-like immunoreactivity in presumptive adrenaline neurones of the fetal rat central nervous system. J Comp Neurol 236:348–381
Heizmann CW (1984) Parvalbumin, an intracellular calcium-binding protein: distribution, properties and possible roles in mammalian cells. Experientia 40:910–921
Heizmann CW, Berchthold MW (1987) Expression of Parvalbumin and other Ca2+-binding proteins in normal and tumor cells: a topical review. Cell Calcium 8:1–41
Heizmann CW, Celio MR (1987) Immunolocalization of parvalbumin. Methods Enzymol 139:552–570
Hsu SM, Raine L, Fanger H (1981) Use of Avidin-Biotin-Peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures. J Histochem Cytochem 29:577–580
Kägi U, Berchthold MW, Heizmann CW (1987) Ca2+-binding parvalbumin in rat testis. Characterization, localization, and expression during development. J Biol Chem 262:7314–7320
Kawaguchi Y, Katsumaru H, Kosaka T, Heizmann CW (1987) Fast spiking cells in the rat hippocampus (CAI region) contain the calcium-binding protein parvalbumin. Brain Res 416:369–374
Kelly J, Whelan CA, Wei DG, Feighery C (1987) Removal of endogenous peroxidase activity from cryostat sections for immunoperoxidase visualization of monoclonal antibodies. J Immunol Methods 96:127–132
Kerns JM (1980) Postnatal differentiation of the rat trochlear nerve. J Comp Neurol 189:291–306
König N, Marty R (1981) Early neurogenesis and synaptogenesis in cerebral cortex. Bibl Anat 19:152–160
Kosaka T, Katsumaru H, Hama K, Wu J-Y, Heizmann CW (1987) GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and denate gyrus. Brain Res 419:119–130
Kretsinger RH (1981) Mechanisms of selective signalling by calcium. Neurosci Res Progr Bull 19(8). MIT Press, Boston
Lance-Jones C (1982) Motoneuron cell death in the developing lumbar spinal cord of the mouse. Dev Brain Res 4:473–479
Landis DMD (1985) Promise and pitfalls in immunocytochemistry. TINS 8:312–317
Lauder JM, Han VKM, Henderson P, Verdoom T, Towle AC (1986) Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience 19:465–493
Lawson SN, Caddy KWT, Biscoe TJ (1974) Development of rat dorsal root ganglion neurones. Cell Tissue Res 153:399–413
Lager DG (1983) Comparative localization of acetylcholinesterase and pseudocholinesterase during morphogenesis of the chicken brain. Proc Natl Acad Sci USA 80:6413–6417
Leong SF, Clark JB (1984) Regional enzyme development in rat brain. Biochem J 218:139–145
Lübbers K, Wolff JR, Frotscher M (1985) Neurogenesis of GABAergic neurons in the rat dentate gyrus: a combined autoradiographic and immunocytochemical study. Neurosci Lett 62:317–322
Matthews MA, Duncan D (1971) A quantitative study of morphological changes accompanying the initiation and progress of myelin production in the dorsal funiculus of the rat spinal cord. J Comp Neurol 142:1–22
McLaughlin BJ, Wood JG, Saito K, Roberts E, Wu J-Y (1975) The fine structural localization of glutamate decarboxylase in developing axonal processes and presynaptic terminals of rodent cerebellum. Brain Res 95:355–371
Means AR, Tash JS, Chafouleas JG (1982) Implications of the presence, distribution, and regulation of calmodulin in eukaryotic cells. Physiol Rev 62:1–39
Michelson HB, Lothman EW (1989) An in-vivo electrophysiological study of the ontogeny of excitatory and inhibitors processes in the rat hippocampus. Dev Brain Res 47:113–122
Mjaatvedt AE, Wong-Riley MTT (1988) Relationship between synaptogenesis and cytochrome oxidase activity in Purkinje cells of the developing rat cerebellum. J Comp Neurol 277:155–182
Morris RJ, Beech JN, Heizmann CW (1988) Two distinct phases and mechanisms of axonal growth shown by primary vestibular fibres in the brain demonstrated by parvalbumin immunohistochemistry. Neuroscience 27:571–596
Mueller AL, Taube JS, Schwartzkroin PA (1984) Development of hyperpolarizing responses to GABA in rabbit hippocampus in vitro. J Neurosci 4:860–867
Nag AC, Cheng M (1982) Differentiation of fibre types in an extraocular muscle of the rat. J Embryol Exp Morphol 71:171–191
Nitsch C, Scotti AL, Sommacal A, Kalt G (1989) GABA-ergic hippocampal neurons resistant to ischemia-induced delayed neuronal death contain the calcium-binding protein parvalbumin. Neurosci Lett 105:263–268
Nitsch R, Bergmann I, Küppers K, Mueller G, Frotscher M (1990) Late appearance of parvalbumin-immunoreactivity in the development of GABA-ergic neurons in the rat hippocampus. Neurosci Lett 118:147–150
Nornes HO, Das GD (1974) Temporal pattern of neurogenesis in spinal cord of the rat. I. An autoradiographic study — time and sites of origin and migration and settling patterns of neuroblasts. Brain Res 73:121–138
Palacios JM, Niehoff DL, Kuhar MJ (1979) Ontogeny of GABA and benzodiazepine receptors: effects of Triton-x100, bromide and muscimol. Brain Res 179:390–395
Purpura DP, Shofer RJ, Scorff T (1965) Properties of synaptic activities and spike potentials of neurons in immature neocortex. J Neurophysiol 28:925–942
Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–84
Rogers J, Khan M, Ellis J (1990) Calretinin and other CaBP's in the nervous system. In: Pochet R, Lawson E, Heizmann CW (eds) Calcium binding proteins in normal and transformed cells. Plenum Press, New York
Schanne FAX, Kane AB, Young EE, Farber JL (1979) Calcium dependence of toxic cell death: a final common pathway. Science 206:700–702
Schwann JW, Brady RJ, Martin DL (1989) Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus. Neuroscience 28:551–561
Séquier JM, Hunziker W, Andressen C, Celio MR (1990) Calbindin D-28k: protein and mRNA localization in the rat brain. Eur J Neurosci 2:1118–1126
Smith CL (1983) The development and postnatal organisation of primary afferent projections to the rat thoracic spinal cord. J Comp Neurol 220:29–43
Sohal GS, Weidman TA (1978) Development of the trochlear nerve: loss of axons during normal ontogeny. Brain Res 142:455–465
Soriano E, Cobas A, Fairén A (1986) Asynchronism in the neurogenesis of GABAergic and non-GABAergic neurons in the mouse hippocampus. Dev Brain Res 30:88–92
Spencer RF, Porter JD (1988) Structural organization of the extraocular muscles. In: Büttner-Ennever JA (ed) Neuroanatomy of the oculomotor system. Elsevier, Amsterdam
Stichel CC, Singer W, Heizmann CW (1988) Light and electron microscopic immunocytochemical localization of parvalbumin in the dorsal lateral geniculate nucleus of the cat: evidence for coexistence with GABA. J Comp Neurol 268:29–37
Vaughn JE, Grieshaber JA (1973) A morphological investigation of an early reflex pathway in developing rat spinal cord. J Comp Neurol 148:177–210
Wolff JR, Balcar VJ, Zetzsche T, Böttcher H, Schmechel DE, Chromwall BM (1984a) Development of GABAergic system in rat visual cortex. In: Lauder JM, Nelson PG (eds) Gene expression and cell-cell interaction in the developing nervous system. Plenum Press, New York, pp 215–239
Wolff JR, Böttcher H, Zetzsche T, Oertel WH, Chromwall BM (1984b) Development of GABAergic neurons in rat visual cortex as identified by glutamate decarboxylase-like immunoreactivity. Neurosci Lett 47:207–212
Zelená J (1957) The morphogenetic influence of innervation on the ontogenetic development of muscle spindle. J Embryol Exp Morphol 5:283–292
Zhang JH, Morita Y, Hironaka T, Emson PC, Tohyama M (1990) Ontological study of Calbindin D-28k-like and Parvalbuminlike immunoreactivities in rat spinal cord and dorsal root ganglia. J Comp Neurol 302:715–728
Ziskind-Conhaim L: (1988) Physiological and morphological changes in developing peripheral nerves of rat embryos. Develop. Brain Res. 42:15–28
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Solbach, S., Celio, M.R. Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat Embryol 184, 103–124 (1991). https://doi.org/10.1007/BF00942742
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DOI: https://doi.org/10.1007/BF00942742