Development and early postnatal maturation of the primary olfactory cortex

doi:10.1016/0165-3806(94)90093-0

Developmental Brain Research

Volume 80, Issues 1–2, 15 July 1994, Pages 96-114

https://doi.org/10.1016/0165-3806(94)90093-0 Get rights and content

Abstract

Tritiated thymidine autoradiography was used to study the origin and distribution of neurons in the primary olfactory cortex of the rat. The principal interest was devoted to animals injected at embryonic day 12 (E12) and sacrificed at different pre- and postnatal ages. The first generated neurons appearing at E12 were studied from E15 to P63. Animals sacrificed at E15 show a group of heavily labeled cells occupying a large area of the ventro lateral region of the telencephalic vesicle. At E16 this group differentiates into the principal cells of the accessory olfactory bulb and cells of the prospective primary olfactory cortex (POC). At E18-E20 the ventral tip of the cortical plate apparently divides this group into a superficial part corresponding to layer I and a deep part, corresponding to cells located in the adult in layer III. Labeled cells in layer I were found flanking the lateral olfactory tract (TOL), but rarely in the adult suggesting that they disappear or transform postnatally. Golgi observations were carried out from E15 to postnatal day 8. The morphology of different cells were studied. Layer I contains polymorphic cells resembling Cajal-Retzius cells. Among other cell types, layer II includes kinds of pyramidal cells lacking basal dendrites known as semilunar cells and intrinsic neurons. Layer III contains pyramidal cells having more than one apical dendrite ascending to the surface.

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The characteristics of muscarinic acetylcholine receptor agonist-induced epileptiform bursting seen in immature rat piriform cortex slices in vitro were further investigated using intracellular recording, with particular focus on its postnatal age-dependence (P+14–P+30), pharmacology, site(s) of origin and the likely contribution of the muscarinic acetylcholine receptor agonist-induced post-stimulus slow afterdepolarization and gap junction functionality toward its generation. The muscarinic agonist, oxotremorine-M (10μM), induced rhythmic bursting only in immature piriform cortex slices; however, paroxysmal depolarizing shift amplitude, burst duration and burst incidence were inversely related to postnatal age. No significant age-dependent changes in neuronal membrane properties or postsynaptic muscarinic responsiveness accounted for this decline. Burst incidence was higher when recorded in anterior and posterior regions of the immature piriform cortex. In adult and immature neurones, oxotremorine-M effects were abolished by M1-, but not M2-muscarinic acetylcholine receptor-selective antagonists. Rostrocaudal lesions, between piriform cortex layers I and II, or layer III and endopiriform nucleus in adult or immature slices did not influence oxotremorine-M effects; however, the slow afterdepolarization in adult (but not immature) lesioned slices was abolished. Gap junction blockers (carbenoxolone or octanol) disrupted muscarinic bursting and diminished the slow afterdepolarization in immature slices, suggesting that gap junction connectivity was important for bursting. Our data show that neural networks within layers II–III function as primary oscillatory circuits for burst initiation in immature rat piriform cortex during persistent muscarinic receptor activation. Furthermore, we propose that muscarinic slow afterdepolarization induction and gap junction communication could contribute towards the increased epileptiform susceptibility of this brain area.

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Research reportDevelopment and early postnatal maturation of the primary olfactory cortex

Abstract

Int. J. Dev. Neurosci.

Exp. Neurol.

Exp. Neurol.

Neuroscience

Brain Res. Bull.

Brain Res.

Dev. Biol.

Neuroscience

Neuroscience

Neurosci. Lett.

Neuron

Dev. Brain Res.

Dev. Brain Res.

Brain Res.

Neuroscience

Neuroscience

3H-Thymidine-radiographic studies of neurogenesis in the rat olfactory bulb

Exp. Brain Res.

Development of olfactory and related structures in staged human embryos

Anat. Embryol.

Olfactory relationships of the telencephalon and diencephalon in the rabbit. I. An autoradiographic study of the efferent connections of the main and accessory olfactory bulbs

J. Comp. Neurol.

The effects of the removal of the nasal pits in Amblystoma embryos

J. Exp. Zool.

The quantitative relationship between olfactory axons and mitral/tufted cells in developing Xenopus with partially deafferented olfactory bulbs

J. Neurobiol.

Development of the prosencephalon

Connections of the olfactory bulb and nucleus olfactorius anterior in the hedgehog (Erinaceus europaeus): fluorescent tracers and HRP study

J. Comp. Neurol.

Cells coming from the olfactory placode may induce the development of the telencephalic vesicles

Soc. Neurosci. Abstr.

Fiber trajectories of olfactory bulb efferents in the hamster

J. Comp. Neurol.

The cells of Cajal-Retzius in the developing human brain

J. Anat.

Initial tract formation in the mouse brain

J. Neurosci.

Autoradiographic study of development of the cerebral cortex in the rabbit

Brain Behav. Evol.

Dispersion of neural progenitors within the germinal zones of the forebrain

Nature

Early postnatal cellular proliferation and survival in the olfactory bulb and rostral migratory stream of normal and odor deprived rats

J. Comp. Neurol.

Age-dependent cell death in the olfactory cortex: lack of transneuronal degeneration in neonates

J. Comp. Neurol.

The human transient subpial granular layer: an optical, immunohistochemical, and ultrastructural analysis

J. Comp. Neurol.

Anomalies des nerfs olfactifs et origine du bulbe olfactif

C.R. Séances Soc. Biol.

Implications of the “initial brain” concept for brain evolution in cetacea

Behav. Brain Sci.

Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons

J. Neurocytol.

Structure of the piriform cortex of the opossum. I. Description of neuron types with Golgi methods

J. Comp. Neurol.

The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat

Brain Res.

Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and olfactory areas

J. Comp. Neurol.

Association and commissural fiber systems of the olfactory cortex of the rat. II. Systems originating in the olfactory peduncle

J. Comp. Neurol.

Rapid transneuronal degeneration and death of cortical neurons following removal of the olfactory bulb in adult rats

J. Comp. Neurol.

Autoradiographic study of histogenesis in the mouse olfactory bulb. II. Cell proliferation and migration

J Comp. Neurol.

Autoradiographic study of histogenesis in the area pyriformis and claustrum of the mouse

Anat. Rec.

Research report
Development and early postnatal maturation of the primary olfactory cortex

³H-Thymidine-radiographic studies of neurogenesis in the rat olfactory bulb