Migration of LHRH-immunoreactive neurons from the olfactory placode rationalizes olfacto-hormonal relationships

doi:10.1016/0960-0760(91)90254-3

The Journal of Steroid Biochemistry and Molecular Biology

Volume 39, Issue 4, Part 2, October 1991, Pages 565-572

https://doi.org/10.1016/0960-0760(91)90254-3 Get rights and content

Abstract

Nerve cells that express luteinizing hormone-releasing hormone (LHRH), essential for reproductive functions, originate in the epithelium of the medial olfactory placode. While the peripheral origin of this physiologically important brain peptide is surprising, associations between olfactory and reproductive systems are well documented in behavioral studies of pheromones and in clinical studies of disorders including hypogonadotropic hypogonadism with anosmia or olfactory-genital dysplasia. Mechanisms underlying this migration include a close association with neural cell adhesion molecules (NCAM), but are likely also to involve other physical and chemical factors.

References (59)

M. Schwanzel-Fukuda et al.
The fetal development of the luteinizing hormone-releasing hormone (LHRH) neuronal systems of the guinea pig brain
Brain Res. Bull
(1981)
L. Muske et al.
Ontogeny of immuno-reactive gonadrotropin-releasing hormone neuronal systems in amphibians
Brain Res.
(1990)
S. Wray et al.
Spatiotemporal cell expression of luteinizing hormone-releasing hormone in the prenatal mouse: evidence for an embryonic origin in the olfactory placode
Dev. Brain Res.
(1989)
H. Daikoku-Ishido et al.
Development of the hypothalamic luteinizing hormone-releasing hormone-containing neuron system in the rat: in vivo and in transplantation studies
Dev. Biol.
(1990)
A.I. Farbman et al.
Early development of olfactory receptor cell axons
Dev. Brain Res.
(1985)
A. Mroueh et al.
Olfacto-genital dysplasia
Am. J. Obstet. Gynec.
(1968)
M. Schwanzel-Fukuda et al.
Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome
Molec. Brain Res.
(1989)
J. Barry
Characterization and topography of LHRH neurons in the human brain
Neurosci. Lett.
(1976)
A.V. Schally et al.
Gonadotropin-releasing hormone: one polypeptide regulates secretion of luteinizing hormone and follicle-stimulating hormone
Science
(1971)
R. Guillemin
Peptides in the brain: the new endocrinology of the neuron
Science
(1978)

R.L. Moss et al.

Induction of mating behavior in rats by luteinizing hormone-releasing factor

Science

(1973)

D.W. Pfaff

Luteinizing hormone-releasing factor potentiates lordosis behavior in hypophysectomized ovariectomized female rats

Science

(1973)

A.-J. Silverman

The gonadotropin-releasing hormone (GnRH) neuronal systems: immunocytochemistry

O. Larsell

The nervus terminalis

Ann. Otol. Rhinol. Laryng.

(1950)

F. Bojsen-Moller

Demonstration of the terminalis, olfactory, trigeminal and perivascular nerves in the rat nasal septum

J. Comp. Neurol.

(1978)

M. Schwanzel-Fukuda et al.

The nervus terminalis of the guinea pig: a new LH-RH neuronal system

J. Comp. Neurol.

(1980)

J.W. Witkin et al.

Luteinizing hormone-releasing hormone in rat olfactory systems

J. Comp. Neurol.

(1983)

M. Schwanzel-Fukuda et al.

Ontogenesis of neurons producing luteinizing hormone-releasing hormone

J. Comp. Neurol.

(1985)

L. Jennes et al.

Luteinizing hormone-releasing hormone (LHRH) systems in the brain of the golden hamster

Cell Tiss. Res.

(1980)

M. Schwanzel-Fukuda et al.

Distribution of luteinizing hormone-releasing hormone in the nervus terminalis and brain of the mouse detected by immunocytochemistry

J. Comp. Neurol.

(1985)

M. Schwanzel-Fukuda et al.

Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) in the brain and nervus terminalis of the adult and early neonatal gray short-tailed opossum

J. Comp. Neurol.

(1988)

J.W. Witkin

Luteinizing hormone-releasing hormone (LHRH) in olfactory systems in primates

S.H. Ridgway et al.

The terminal nerve in odontocete cetaceans

L.S. Demski et al.

The terminal nerve of dolphins: gross structure, histology and luteinizing hormone-releasing hormone immunocytochemistry

Brain Behav. Evol.

(1990)

O. Ronnekleiv et al.

Ontogeny of gonatropin-releasing hormone-containing neurons in early fetal development of rhesus macaques

Endocrinology

(1990)

L.R. Halpern-Sebold et al.

Ontogeny of centers containing luteinizing hormone-releasing hormone in the brain of the platyfish (Xiphophorus maculatus) as determined by immunocytochemistry

Cell Tiss. Res.

(1983)

H. Münz et al.

The terminal nerve and its development in teleost fishes

L. Muske et al.

Luteinizing hormone-releasing hormone immunoreactive neurons in the amphibian brain are distributed along the course of the nervus terminalis

L. Muske et al.

The nervus terminalis in amphibians: anatomy, chemistry and relationship with the hypothalamic gonadotropin-releasing hormone system

Brain Behav. Evol.

(1988)

Cited by (36)

Daniel S. Lehrman Lifetime Achievement Award. Sex in the brain: Donald Wells Pfaff and motivation from genes to molecules to behavior.
2012, Hormones and Behavior
Citation Excerpt :
Another seminal discovery of Don Pfaff's laboratory is the first demonstration of a phenomenon that is today found in every textbook of physiology: that gonadotropin-releasing hormone (GnRH) neurons that control the development and activity of the gonads do not initially form in the hypothalamus. Rather, these cells begin expressing GnRH while in the olfactory pit and subsequently migrate to the basal forebrain (Schwanzel-Fukuda and Pfaff, 1989, 1992; Schwanzel-Fukuda et al., 1992, 1994, 1996). Not only has this discovery changed the way we all think about the development of the reproductive system, but it has also explained the seemingly oddly combined symptoms of X chromosome-linked Kallmann's syndrome: hypogonadism and anosmia (Schwanzel-Fukuda et al., 1989).
The gonadotropin-releasing hormone and its receptor
2009, Hormones, Brain and Behavior Online
Gonadotropin-releasing hormone (GnRH) is the central neuropeptide in vertebrates that controls the synthesis and release of luteinizing hormone and follicle-stimulating hormone in the anterior pituitary. Its prevalence suggests that it is required for the reproductive success of many species. It is therefore important to understand the factors that control the synthesis and release of GnRH in the brain as well as the mechanisms by which GnRH controls the responses of its targets in the central nervous system and in the anterior pituitary. This chapter focuses on the development and anatomy of the GnRH neuronal system; some of the actions and mechanisms that regulate GnRH neurons; and the localization, regulation, and functional aspects of GnRH receptors in the brain. Finally, the mechanisms of action of GnRH in the anterior pituitary or pituitary-derived cell lines are discussed.
Pheromones and mammalian reproduction
2006, Knobil and Neill's Physiology of Reproduction
Ontogeny of GnRH-like immunoreactive neuronal systems in the forebrain of the Indian major carp, Cirrhinus mrigala
2005, General and Comparative Endocrinology
GnRH immunoreactivity appeared in the medial olfactory placode very early in the development of Cirrhinus mrigala. The immunoreactive elements were divisible into distinct migratory and non-migratory components. The migratory component appeared as a patch of intensely immunoreactive cells located close to the olfactory epithelium in day 6 post-fertilization larvae. Subsequently, these neurons migrate caudally along the ventromedial aspect of the developing forebrain and enroute give rise to GnRH immunoreactive neurons in the (1) nervus terminalis located in ventral and caudal part of the olfactory bulb (day 8), and (2) basal telencephalon (day 9). The non-migratory GnRH immunoreactive component appeared in the olfactory placode of day 1 post-fertilization larvae. It consisted of few olfactory receptor neuron (ORN)-like cells with distinct flask-shaped somata, dendrites that communicate with the periphery and a single axon on the basal side; GnRH immunoreactivity was seen throughout the neuron. Considerable increase in the number of immunoreactive ORNs was encountered in day 2 post-fertilization larvae. On day 3, the dendrites of ORNs sprout bunches of apical cilia, while on the basal side the axonal outgrowths can be traced to the olfactory bulb. GnRH immunoreactive fibers were distributed in the olfactory nerve layer in the periphery of the bulb and glomeruli-like innervation was clearly established in 5 days old larvae. The innervation to the olfactory bulb showed a considerable increase in GnRH immunoreactivity in 9 and 19 days old larvae. However, GnRH immunoreactivity in non-migratory as well as migratory components gradually diminished and disappeared altogether by the age of 68 days. Results of the present study suggest that GnRH may serve a neurotransmitter role in the ORNs during early stages of development in C. mrigala.
Pheromones and Mammalian Reproduction
2005, Knobil and Neill's Physiology of Reproduction
Olfactory regulation of maternal behavior in mammals
2004, Hormones and Behavior
In mammals, olfactory cues are extensively used in many aspects of maternal care to ensure the coordination of mother–infant interactions and consequently the normal development of the offspring. Outside the period of parturition and lactation, when the young are not a behavioral priority, olfactory cues play an inhibitory role on maternal responsiveness since in most mammalian species studied so far, nonpregnant females find the odor of young aversive. On the contrary at the time of parturition, a shift in the hedonic value of infantile odors occurs so that the young now become a very potent stimulus and this sensorial processing constitutes an important part of the maternal motivational system. Moreover, infants' odors provide a basis for individual recognition by their mothers and some species (ungulates) have developed highly specialized mechanisms for processing of the infant signals. Perception of the smell of the young also regulates various aspects of maternal behavior. Dodecyl propionate, a compound released by of pup's preputial glands, has been shown to influence anogenital licking behavior, a fundamental pattern of maternal behavior in rodents. While there is no functional specificity of either the main or the accessory olfactory systems in the development of maternal behavior amongst species, it appears that only the main olfactory system is implicated when individual odor discrimination of the young is required. Neural structures, such as the main olfactory bulb, undergo profound changes when exposed to offspring odors at parturition. These changes in synaptic circuitry contribute both to maternal responsiveness to these odors, to their memorization, and to effects of long-term maternal experience.

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Migration of LHRH-immunoreactive neurons from the olfactory placode rationalizes olfacto-hormonal relationships

Abstract

Brain Res. Bull

Brain Res.

Dev. Brain Res.

Dev. Biol.

Dev. Brain Res.

Am. J. Obstet. Gynec.

Molec. Brain Res.

Neurosci. Lett.

Gonadotropin-releasing hormone: one polypeptide regulates secretion of luteinizing hormone and follicle-stimulating hormone

Science

Peptides in the brain: the new endocrinology of the neuron

Science

Induction of mating behavior in rats by luteinizing hormone-releasing factor

Science

Luteinizing hormone-releasing factor potentiates lordosis behavior in hypophysectomized ovariectomized female rats

Science

The gonadotropin-releasing hormone (GnRH) neuronal systems: immunocytochemistry

The nervus terminalis

Ann. Otol. Rhinol. Laryng.

Demonstration of the terminalis, olfactory, trigeminal and perivascular nerves in the rat nasal septum

J. Comp. Neurol.

The nervus terminalis of the guinea pig: a new LH-RH neuronal system

J. Comp. Neurol.

Luteinizing hormone-releasing hormone in rat olfactory systems

J. Comp. Neurol.

Ontogenesis of neurons producing luteinizing hormone-releasing hormone

J. Comp. Neurol.

Luteinizing hormone-releasing hormone (LHRH) systems in the brain of the golden hamster

Cell Tiss. Res.

Distribution of luteinizing hormone-releasing hormone in the nervus terminalis and brain of the mouse detected by immunocytochemistry

J. Comp. Neurol.

Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) in the brain and nervus terminalis of the adult and early neonatal gray short-tailed opossum

J. Comp. Neurol.

Luteinizing hormone-releasing hormone (LHRH) in olfactory systems in primates

The terminal nerve in odontocete cetaceans

The terminal nerve of dolphins: gross structure, histology and luteinizing hormone-releasing hormone immunocytochemistry

Brain Behav. Evol.

Ontogeny of gonatropin-releasing hormone-containing neurons in early fetal development of rhesus macaques

Endocrinology

Ontogeny of centers containing luteinizing hormone-releasing hormone in the brain of the platyfish (Xiphophorus maculatus) as determined by immunocytochemistry

Cell Tiss. Res.

The terminal nerve and its development in teleost fishes

Luteinizing hormone-releasing hormone immunoreactive neurons in the amphibian brain are distributed along the course of the nervus terminalis

The nervus terminalis in amphibians: anatomy, chemistry and relationship with the hypothalamic gonadotropin-releasing hormone system

Brain Behav. Evol.