Table Of ContentOntogeny
of Olfaction
Principles of Olfactory Maturation
in Vertebrates
Edited by Winrich Breipohl
With 78 Figures
Springer-Verlag
Berlin Heidelberg New York
London Paris Tokyo
Editor:
Professor Dr. WINRICH BREIPOHL
Department of Anatomy, University of Queensland
St. LucialBrisbane, Australia 4067
Co-Editor:
Professor Dr. RAIMUND APFELBACH
Institut fur Biologie III, Universitat Tubingen
7400 Tubingen, FRG
Editorial Assistants:
MARIAN KREMER, Institut fUr Anatomie
Universitatsklinikum Essen, 4300 Essen, FRG
BRIAN KEY, Department of Anatomy
University of Queensland, St. Lucia/Brisbane
Australia 4067
MICHAEL RAUWOLF, Institut fUr Anatomie
Universitatsklinikum Essen, 4300 Essen, FRG
ISBN-13: 978-3-642-71578-5 e-ISBN-13: 978-3-642-71576-1
001: 10.1007/978-3-642-71576-1
Library of Congress Cataloging in Publication Data. Ontogeny of olfaction. Includes index.
1. Smell. 2. Ontogeny. I. Breipohl, W. [DNLM: 1. Central Nervous System-growth & develop
ment. 2. Olfactory Bulb-growth & development. 3. Olfactory Mucosa-growth & development.
WV 301059] QP458.058 1986 596',01'826 86-22113
This work is subject to copyright. All rights are reserved, whether the whole or part of the
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Under § 54 of the German Copyright Law, where copies are made for other than private use, a
fee is payable to "Verwertungsgesellschaft Wort", Munich.
© Springer-Verlag Berlin Heidelberg 1986
Softcover reprint of the hardcover I st edition 1986
The use of registered names, trademarks, etc. in this publication does not imply, even in the
absence of a specific statement, that such names are exempt from the relevant protective laws
and regulations and therefore free for general use.
2131/3130-543210
This book is dedicated to my former colleagues, coworkers, and friends in the
Medical Faculty at the University of Essen (FRG) and to my new colleagues and
coworkers at the University of Queensland (Australia).
PREFACE
The impacts of specifically experienced external and internal environments upon
phylogenetically established pathways of ontogenetic development seem to be
responsible for the intra-species variation of organisms. Therefore normal
function, as well as disorders of sensory systems, can often be better understood
by considering the principles of ontogenetic maturation and the time schedule of
environmental influences during that period.
Sensory organs and systems have long been considered to be hereditally determin
ed for their analysis of the environment. However, it is becoming more and more
clear that their specificity depends also upon the sequence and nature of environ
mental impacts, impacts during highly sensitive periods of postnatal life being
most effective.
The present book, using an interdisciplinary approach, has brought together
various descriptions of developmental processes for one of the phylogenetically
oldest sensory analytical circuits, the olfactory system. Although investigations of
a wide range of vertebrates are included, from marsupials to man, the main
attention was given to rodents, the most frequently used experimental animal in
this fields of research. Authors have been asked for reviews and original
considerations on the rationales of developmental principles in the olfactory
system, and wherever appropriate to highlight its uniqueness or similarities with
other parts of the nervous system. Authors were also asked to consider future
needs of research in their fields, to describe their own approaches in this
context, and to outline general horizons of neurodevelopmental research. As a
result the book contains many new sophisticated explanations of the maturation
and function of the olfactory system, with several articles presenting data which
highlight urgent needs to modify some present hypotheses.
Although being aware of the Sysiphos-like type of all scientific investigations and
the relativity of knowledge, I hope that this collection of articles may lead to
better understanding of the role of inborn and acquired features for the normal
structure and function as well as disorders of the vertebrate nervous system in
general and the olfactory system in particular. This book, hopefully, may also
stimulate the reader's scientific enjoyment and encourage his own future
contributions in this field of neurobiology.
Winrich Breipohl
CONTENTS
A. INTRODUCTION
1. Ontogeny of Human Olfactory Function
RL Doty (with 7 Figure) .••..••.•••••••••.•••••••.••••••••••••••. 3
B. PRltlCIPLES OF NEURONAL CELL PROLIFERATION
2. Neurogenesis in the Vertebrate Main Olfactory Epithelium
W Breipohl, A Mackay-Sim, D Grandt, B Rehn, C Darrelmann
(with 2 Figures) •••..•.••.••.•••••.•••••...•••.••.•••••.•••••.••. 21
3. Effects of Sex Steroids on the Development of the
Vomeronasal System in the Rat
S Segovia, A Guillamon (with 7 Figure).. .•.•• •....•.• ••.•••. •.••. 35
C. MORPHOLOGICAL MATURATION OF THE OLFACTORY PERIPHERY
4. Development of Olfactory Epithelium in the Rat
AI Farbman, BPhM Menco (with 6 Figures) •.••.•••••••••••••••••• 45
5. Morphological Maturation of the Olfactory Epithelia
of Australian Marsupials
JE Kratzing (with 3 Figures) ..•••••••.••••••••••••••••••••.•••••• 57
6. Ontogeny of the Secretory Elements in the Vertebrate
Olfactory Mucosa
l\1L Getchell, B Zielinski, TV Getchell (with 9 Figures) 71
7. Developmental Studies on Enzyme Histochemistry of the
Three Olfactory Epithelia in the Golden Hamster
Kazuyuki Taniguchi, Kazumi Taniguchi, Shin-ichi Mikani
(with 6 Figures) .•••.••••..•••.•••.•••..•...••.•..•.•••••••••...• 83
8. Immunocytochemical Studies on the Maturation of the Rodent
Olfactory Mucosa
J /;1organ......................................................... 95
D. POSTNATAL MATURATION OF THE OLFACTORY BULB
9. Ontogeny of Carnosine, Olfactory Marker Protein and
Neurotransmitter Enzymes in Olfactory Bulb and Mucosa
of the Rat
FL Margolis, T Kawano, IA Grillo (with 5 Figures) ••••...•.••..•.. 107
x
10. Electrophysiological Investigations on the Development
of the Olfactory System in Laboratory ~~ice
U Schmidt (with 6 Figures)....................................... 117
11. The Effect of Long Duration Postnatal Odour Exposure
on the Development of the Rat Olfactory Bulb
H Panhuber (with 5 Figures) . .• ...... . •.• ....••.••..•• •••. .•. .... 127
12. Transient Postnatal Impacts on the Olfactory Epithelium
Proprium Affect the Granule Cell Development in the Mouse
Olfactory Bulb
B Rehn, W Breipohl (with 8 Figures)............................. 143
13. Central and Peripheral Influences on Postnatal Growth and
Development of the Olfactory Bulb in the Rat
E Meisami (with" Figures) ...••..........................•.....•. 157
E. MATURATION OF TERTIARY OLFACTORY CENTERS
14. Development of Axonal Connections in the Central
Olfactory System
J E Schwob, B Friedman, JL Price (with 9 Figures) 177
15. Impacts of Postnatal Olfactory Deprivation on the
Amygdaloid Complex in Mouse
ZB Lu, W Breipohl, B Rehn (with 1 Figure) ••••.................. 199
16. Structure and Development of the LHRH-Immunoreactive
Nucleus Olfacto-Retinalis in the Cichlid Fish Brain
MD Crapon de Caprona, H Munz, B Fritzsch, B Claas
(with" Figures) •.....••....................•..•••..•.••••...•.•. 211
F. POSTNATAL DEVELOPMENT OF OLFACTORY-GUIDED BEHAVIOR
17. Postnatal Development of Olfactory-Guided Behavior
in Rodents
JR Alberts....................................................... 227
18. Neurobehavioral Analysis of Odor Preference Development
in Rodents
R Coopersmith, M Leon........................................... 237
19. Olfactory Guidance of Nipple-Search Behaviour in
Newborn Rabbits
R Hudson, H Distel (with 5 Figures) .•......•............••...... 243
20. Salivary Pheromones in the Pig and Human in Relation
to Sexual Status and Age
DB Gower, WD Booth (with 3 Figures)............................ 255
Subject Index 265
LIST OF CONTRIBUTORS
Alberts JR 227 Kratzing JE 57
Booth WD 255 Leon M 237
Breipohl W 21 Lu ZB 199
Claas B 211 Mackay-Sim A 21
Coopersmith R 237 Margolis FL 107
Crapon de Caprona MD 211 Meisami E 157
Darrelmann C 21 Menco BPhM 45
Distel H 243 Mikani S 83
Doty RL 3 Morgan J 95
Farbman AI 45 Munz H 211
Friedman B 177 Panhuber H 127
Fritzsch B 211 Price JL 177
Getchell ML 71 Rehn B 143
Getchell TV 71 Schmidt U 117
Gower DB 255 Schwob JE 177
Grandt D 21 Segovia S 35
Grillo M 107 Taniguchi Kazuyuki 83
Guillamon A 35 Taniguchi Kazumi 83
Hudson R 243 Zielinski B 71
Kawano T 107
A. INTRODUCTION
Ontogeny of Human Olfactory Function
RL Doty
Smell and Taste Center, Department of Otorhinolaryngology and Human
Communication, and Department of Physiology, School of Medicine, University of
Pennsylvania, Philadelphia, PA 19104, USA
1 Introduction
Until recently, little was known about the onset of olfactory function in humans or
about the nature of alterations in smell function across the lifespan. Unequivocal
answers to such basic questions as to whether neonates can detect odorants (in
dependent of trigeminal stimulation) or to what degree smell ability declines in old
age were not available. During the last decade a number of behavioral studies
have provided definitive answers to such questions, ushering in a new era of
human behavioral research. This research, complemented by anatomical studies,
indicates that the human olfactory system is operative at birth and that massive
loss of smell function occurs in many older individuals. However, as will be
addressed in this chapter, numerous other questions concerning the nature of
age-related changes in human olfactory function remains unanswered.
2 Olfaction in the Neonate
2.1 Anatomical Considerations
The olfactory neuroepithelium is well developed in the human fetus, with cilia
appearing from olfactory knobs by 9 weeks. By 11 weeks completely differentiated
olfactory cells are observed (pyatkina 1982). Adult-like lamination of the olfactory
bulb is seen at 18.5 weeks (Humphrey 1940). Both periglomerular and inter
glomerular cells are seen at this early stage, as is a well-defined granule cell
layer • However, olfactory marker protein is not yet present in the 22-week
fetus, even though it is present in the adult (Nakashima et al. 1985). This
lThe appearance of the granule cells at this early stage is unlike the situation in
rats and mice, where a large proportion of these cells make their appearance
after birth, originating as late as several weeks postnatally (Altman 1969; Altman
and Das 1966; Hinds 1968 a,b). Apparently the full compliment of granule and
periglumerular cells is not needed for many early olfactory functions, since
newborn rats use odor cues in suckling and can be readily conditioned to
approach or avoid novel odors (Blass et al. 1977; Rudy and Cheatle 1977).
Furthermore fetal rats (gestational day 20) that have received in utero injections
of apple juice and lithium chloride show postpartum evidence of having developed
a conditioned aversion to the odor of apple juice (Smotherman 1982) (for review,
see Doty 1985b).
