Summary
The cholinergic innervation of the rat cerebral cortex was examined in pre- and postnatal life using immunohistochemistry with a monoclonal antibody directed against choline acetyltransferase (ChAT). Our observations show that there are two separate phases in the development of the cholinergic innervation of the rat neocortex. The first, a transient phase, occurs in the late stages of gestation and in the perinatal period. During this time, ChAT-labelled cells (neuroblasts, as well as immature pyramidal and non-pyramidal neurons) are present throughout the entire rostro-caudal extent of the primordial cortex. The fate of these cells, which are not visible shortly after birth, is unknwon as is their functional role in the developing cortex. The second phase in the development of the cholinergic innervation begins in the middle of the second postnatal week. At this stage only a few faintly stained neurons and fibres appear in the cortex. Their numbers and staining intensity increase gradually until the fifth postnatal week when ChAT-labelled neurons and axonal arbours appear indistinguishable from their adult counterparts. The pattern of development observed in the second phase parallels closely that shown in a recent analysis of cortical ChAT activity during postnatal life.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Armstrong DM, Bruce G, Hersch LB, Gage FH (1987) Development of cholinergic neurons in the septal/diagonal band complex of the rat. Dev Brain Res 36:249–256
Bear MF, Carnes KM, Ebner FF (1985) Postnatal changes in the distribution of acetylcholinesterase in kitten striate cortex. J Comp Neurol 237:519–532
Bigl V, Woolf NJ, Butcher LL (1982) Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital and cingulate cortices: a combined fluorescent tracer and acetylcholinsterase analysis. Brain Res Bull 8:727–749
Carey RG, Rieck RW (1987) Topographic projections to the visual cortex from the basal forebrain in the rat. Brain Res 424:205–215
Cavanagh ME, Parnavelas JG (1988) Development of somatostatin immunoreactive neurons in the rat occipital cortex: a combined immunocytochemical-autoradiographic study. J Comp Neurol 268:1–12
Dinopoulos A, Eadie LA, Dori I, Parnavelas JG (1989) The development of basal forebrain projections to the rat visual cortex. Exp Brain Res (in press)
Eckenstein F, Barde Y-A, Thoenen H (1981) Production of specific antibodies to choline acetyltransferase purified from pig brain. Neuroscience 6:993–1000
Eckenstein F, Thoenen H (1982) Production of specific antisera and monoclonal antibodies to choline acetyltransferase: characterization and use for identification of cholinergic neurons. EMBO J 1:363–368
Eckenstein F, Baughman RW (1984) Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature 309:153–155
Eckenstein FP, Baughman RW, Quinn J (1988) An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience 25:457–474
Fosse VM, Kvale I, Lund-Karlsen R, Fonnum F (1984) Postnatal neurochemical development of the rat visual system. In: Sharma SC (ed) Organizing principles of neural development. Plenum Press, New York, pp 187–203
Foster GA, Schultzberg M (1984) Immunohistochemical analysis of the ontogeny of neuropeptide Y immunoreactive neurons in foetal rat brain. Int J Dev Neurosci 2:387–407
Gould E, Butcher LL (1987) Transient expression of choline acetyltransferase-like immunoreactivity in Purkinje cells of the developing rat cerebellum. Dev Brain Res 34:303–306
Hedreen JC, Bacon SJ, Cork LC, Kitt CA, Crawford GD, Salvaterra PM, Price DL (1983) Immunocytochemical identification of cholinergic neurons in the monkey central nervous system using monoclonal antibodies against choline acetyltransferase. Neurosci Lett 43:173–177
Hendry SHC, Jones EG, Killackey HP, Chalupa LM (1987) Choline acetyltransferase-immunoreactive neurons in fetal monkey cerebral cortex. Dev Brain Res 37:313–317
Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1985) Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J Comp Neurol 234:17–34
Kostovic I, Rakic P (1984) Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci 4:25–42
Krnjević K, Silver A (1966) Acetylcholinesterase in the developing forebrain. J Anat 100:63–89
Kvale I, Fosse VM, Fonnum F (1983) Development of neurotransmitter parameters in lateral geniculate body, superior colliculus and visual cortex of the albino rat. Dev Brain Res 7:137–145
Lysakowski A, Wainer BH, Rye DB, Bruce G, Hersch LB (1986) Cholinergic innervation displays strikingly different laminar preferences in several cortical areas. Neurosci Lett 64:102–108
McDonald JK, Parnavelas JG, Karamanlidis AN, Brecha N (1982) The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. II. Vasoactive intestinal polypeptide. J Neurocytol 11:825–837
McDonald JK, Speciale SG, Parnavelas JG (1987) Laminar distribution of glutamate decarboxylase and choline acetyltransferase in the adult and developing visual cortex of the rat. Neuroscience 21:825–832
Mesulam M-M, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185–1201
Mesulam M-M, Mufson EJ, Levey AI, Wainer BH (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12:669–686
Parnavelas JG, Kelly W, Franke E, Eckenstein F (1986) Cholinergic neurons and fibres in the rat visual cortex. J Neurocytol 15:329–336
Parnavelas JG, Cavanagh ME (1988) Transient expression of neurotransmitters in the developing neocortex. Trends Neurosci 11:92–93
Robertson RT (1987) A morphogenetic role for transiently expressed acetylcholinesterase in developing thalamocortical systems? Neurosci Lett 75:259–264
Saper CB (1984) Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J Comp Neurol 222:313–342
Shute CCD, Lewis PR (1967) The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. Brain 90:497–520
Wenk H, Bigl V, Meyer U (1980) Cholinergic projections from magnocellular nuclei of the basal forebrain to cortical areas in rats. Brain Res Rev 2:295–316
Wahle P, Meyer G (1987) Morphology and quantitative changes of transient NPY-ir neuronal populations during early postnatal development of the cat visual cortex. J Comp Neurol 261:165–192
Woodhams PL, Allen YS, McGovern J, Allen JM, Bloom SR, Balazs R, Polak JM (1985) Immunohistochemical analysis of the early ontogeny of the neuropeptide Y system in the rat brain. Neuroscience 15:173–202
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Dori, I., Parnavelas, J.G. The cholinergic innervation of the rat cerebral cortex shows two distinct phases in development. Exp Brain Res 76, 417–423 (1989). https://doi.org/10.1007/BF00247899
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00247899