Table Of ContentComparative Brain Research in Mammals
Volume 1
Heinz Stephan Georg Baron Heiko D. Frahm
Insectivora
With a Stereotaxic Atlas of the Hedgehog Brain
With 129 Figures
Springer-Verlag
New York Berlin Heidelberg London
Paris Tokyo Hong Kong Barcelona
Heinz Stephan Georg Baron
Max-Planck-Institut fUr Hirnforschung Departement de Sciences Biologiques
6000 Frankfurt a.M. 71 (Niederrad) Universite de Montreal
Federal Republic of Germany Montreal, Quebec H3C 317
Canada
Heiko D. Frahm
Anatomisches Institut der UniversiHit
5000 Kaln 41
Federal Republic of Germany
Cover art: Top, Figure 16, page 37, Tenrec ecaudatus; middle, Figure 19, page 37, Potamogale
velox; bottom, Figure 20, page 38, Chrysochloris stuhlmanni.
Library of Congress Cataloging-in-Publication Data
Insectivora/ Heinz Stephan, Georg Baron, Heiko D. Frahm
p. cm. -(Comparative brain research in mammals: v. 1)
Includes bibliographical references and index.
ISBN-13: 978-1-4613-9126-5 e-ISBN-13: 978-1-4613-9124-1
DOl: 10.1007/978-1-4613-9124-1
1. Brain-Physiology. 2. Physiology, Comparative. 3.
Mammals-Physiology. I. Stephan, H. (Heinz), 1924-
II. Baron, G. (Georg), 1930- III. Frahm, Heiko D.
QP376.C627 1991 90-25353
599'.0188-dc20
Printed on acid-free paper.
© 1991 Springer-Verlag New York, Inc.
Softcover reprint of the hardcover I st edition 1991
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9 8 7 6 5 432 1
Editors' Preface
This first volume in the series on "Comparative Brain Research in Mammals"
deals with the brains of Insectivora. The importance of Insectivora lies above
all in the fact that, (1) insectivore-like ancestors are regarded as the initial
group for the evolution of higher mammals, and (2) the insectivore brains
retained many conservative traits, though the animals have adapted to different
living environments. Therefore, the study of Insectivora brains enables an
insight into the size and composition of the brain structure of earlier ancestors
of the higher mammals including primates and humans; in addition, it illumi
nates the various evolutionary trends which made the successful adaptation to
different biotopes possible.
The alterations which the brain has experienced in the course of the phylo
geny and the related adaptive radiation will be examined in the succeeding
volumes on the brains of other Eutheria, e.g., bats (Volume 2) and primates
(Volume 4). In Volume 3 the brains of marsupials will be compared with those
of conservative and evolved Eutheria.
Important topics of this series are the quantitative comparison of the brain
and the discussion of the brain differences with regard to variations in the
biology of the animals. Since all aspects of the life of an animal are directly or
indirectly controlled by the brain, an intimate connection between the structure
of the brain and the behavioral habits of the animal is to be expected. Differ
ences will be discussed in detail, both in view of the brain structures as well as
the taxonomic groups of the animals. Quantitative comparisons are only of
limited worth without presenting the raw data. Otherwise they allow neither a
critical discussion of the original material nor a continuation of the work by
other scientists. The advantage of our data-collection consists above all in the
fact that all histological work follows the same methods and all measurements
follow the same criteria. For this reason the tables are important contents of the
prospective volumes. A large portion of the data presented here is still unpub
lished. The collection of data will be supplemented by a listing of all the
neuroanatomical work on the brains of Insectivora which is known to us. These
studies will be critically evaluated when appropriate. Therefore, the book con
tains (as far as possible) a complete survey of the present knowledge regarding
Insectivora brains.
The series addresses not only the interests of the neuroanatomists or neuro
biologists but also those of scientists interested in ecology, ethology, and
evolution. In the long run, it will be an indispensable source of data for
morphometric studies. The data, which has been collected and worked on for
decades, should retain its validity for a long time.
Contents
1 Introduction 4
Acknowledgements 7
List of the Available Species 7
Abbreviations 8
2 Material and Methods 12
3 Comparative Brain Characteristics 25
3.1 Comparative Macromorphology 25
3.2 Total Brain Size and its Comparison 49
3.3 Comparison of Brain Components 51
3.3.1 Medulla oblongata (OBL) 53
3.3.2 Mesencephalon (MES) 79
3.3.3 Cerebellum (CER) 84
3.3.4 Diencephalon (DIE) 88
3.3.5 Telencephalon (TEL) 100
Main olfactory bulb (MOB) 104
Accessory olfactory bulb (AOB) 107
Paleocortex (PAL) 109
Striatum (STR) 117
Septum (SEP) 119
Amygdala (AMY) 122
Hippocampus (HIP) 127
Schizocortex (SCH) 131
Neocortex (NEO) 132
3.3.6 Comparison with Primates 137
4 Brain Characteristics in Taxonomic Units 158
4.1 Tenrecidae 160
4.1.1 Tenrecinae 160
4.1.2 Geogalinae 166
4.1.3 Oryzorictinae 168
4.1.4 Potamogalinae 171
4.1.5 Summary 176
4.2 Chrysochloridae 185
4.3 Solenodontidae 192
4.4 Erinaceidae 197
4.4.1 Echinosoricinae 197
4.4.2 Erinaceinae 200
4.4.3 Summary 224
Contents 3
4.5 Talpidae 228
4.5.1 Desmaninae 229
4.5.2 Talpinae 234
4.5.3 Summary 250
4.6 Soricidae 254
4.6.1 Soricinae 255
4.6.2 Crocidurinae 270
4.6.3 Summary 281
4.7 Index Profiles of Taxonomic Units 292
5 Adaptive Radiation 298
6 Brain Characteristics Related to Ecoethological Adaptations 312
6.1 Surface Dwellers 312
6.2 Subterranean or Fossorial Species 314
6.3 Semi aquatic Species 315
6.4 Morphological Adaptations for Winter Survival 316
7 Brain Characteristics Related to Functional Systems 318
7.1 Main Olfactory System 318
7.2 Accessory Olfactory (Vomeronasal) System 322
7.3 Visual System 324
7.4 Somatosensory System 327
7.5 Auditory System 330
7.6 Vestibular System 333
7.7 Motor Systems 334
7.8 Limbic System 335
7.9 Neocortex 338
8 Conclusions 341
9 References 344
10 Tables 395
11 Atlas of Atelerix algirus 503
12 Subject Index 554
1 Introduction
The value of the comparative approach as a research strategy lies in the
possibility it offers of examining various aspects of the diversity in nature. For
example, it makes it possible to compare closely related species living in
different ecological conditions as well as different species occupying similar
ecological niches.
Adopting a dynamic approach to morphological studies, in other words,
analyzing the structure of an organism with respect to its ecoethological condi
tions, is not new. However, despite several investigations which tried to relate
the structural organization of particular animals to their living conditions and
activities (e.g., Chapman 1919), consideration of species' natural environments
was long neglected by students of morphology. Boker (1924, 1935, 1937), who
sums up his approach under the term "biological anatomy" (biologische
Anatomie), was perhaps the first to present an integrated view of anatomy as an
ecoethological adaptation. His very promising first attempts unfortunately had
little success because of his adherence to the Lamarckian position (Starck
1978). In the last few decades, however, the assumption that morphological
traits of an organism reflect its ecological niche and that therefore even slight
differences in structure should reflect at least slight differences in function is
gaining acceptance by ecologists. More and more studies have been relating
anatomical features, such as form and size of skeletal structures (e.g., Reed
1951) and shape of hairs (e.g., Hutterer and Hiirter 1981), to ecological aspects
and life style. The ecoethological approach has been particularly fruitful in the
study of chiropteran morphology, as is shown in the summary by Findley and
Wilson (1982). More recently, Hutterer (1985) has given a detailed review of
anatomical adaptations of shrews.
Comparative studies have proven to be particularly fruitful in quantitative
brain research, especially when brain composition is considered. Total brain
size alone may not be sufficient since the same size found in different species
may be the result of a differential growth of different brain parts, e.g., reduc
tion of olfactory structures and simultaneous neocortical enlargement (Stephan
and Andy 1964) or compensatory effects in sensory structures (Jolicoeur and
Baron 1980). Therefore, whenever possible, brain composition should be inves
tigated. As a rule, the size and differentiation of a brain structure do not vary
independently. Increased size is almost always accompanied by progressive
differentiation and vice versa (e.g., Stephan and Andy 1970; Stephan 1975; for
entorhinal cortex and olfactory bulb). The characters of structural differentia
tion can vary in many ways (e.g., in construction, arrangement and connections
of the cells, layers, larger units, etc.), whereas there are only two possibilities
Introduction 5
for variations in size: to become larger or smaller. Thus, an interspecific
comparison of size may serve as a relatively simple first step in determining
the functional importance of a cerebral structure in a given species.
Furthermore, since an animal's interactions with its environment are control
led largely by the nervous system and the size of a given brain structure i.e.,
the amount of brain tissue, is highly interrelated with the functional require
ments of a species' habits, quantitative brain organization should reflect major
evolutionary trends. The brain and its structures have to meet all the external
and internal requirements if the animals and species are to survive. Higher and
more complex behavioral patterns need larger and more differentiated cerebral
structures.
Therefore, analyzing differences in brain structure may not only reveal
trends in brain evolution, but it may ultimately lead to a deeper understanding
of the complex relationship between brain and behavior. Numerous studies in
mammals and birds have shown that variations in the relative size of the entire
brain, of its major regions and, particularly, of specific sensory and motor
nuclei, are paralleled by ecoethological characteristics. For example, in Insec
tivora, the form and size of the brain may change in relation to a particular
substrate adaptation (Spatz and Stephan 1961; Stephan and Spatz 1962). Other
studies have shown that the most reduced olfactory bulbs are found in semi
aquatic forms regardless of their taxonomic affiliation (Stephan and Bauchot
1959; Bauchot and Stephan 1968; Stephan and Kuhn 1982; Baron et al. 1983).
Since, in mammals, olfaction is linked with breathing, it is of no use in
detecting prey under water. Similarly, Bang and Cobb (1968) suggested a
relationship between olfactory ability in various birds and the development of
their olfactory bulbs. Pirlot and Stephan (1970), Stephan and Pirlot (1970),
Pirlot and Pottier (1977) and Stephan et al. (1981 b) were able to establish a
relationship between feeding habits and the size of the total brain and of its
major components in bats. Similarly, Baron (1972, 1974) suggested a relation
ship between the differential development of acoustic nuclei, feeding behavior,
and echolocative abilities in bats and Boire (1989) showed a close correlation
between feeding strategies and the size of the trigeminal and visual brain
centers in birds.
An advantage of quantitative comparisons is that they allow us to rank data.
However, in the absence of other evidence it should not be assumed that such
data rankings represent an evolutionary lineage or historical progression.
Nevertheless, although great caution is required, data rankings may allow
inferences about conservative and derived characters of the brain. The validity
of comparative studies and rank arrangements depends largely on the composi
tion and the size of the sample investigated. The more species studied within a
given taxon, the greater the likelihood of revealing the whole extent of adaptive
radiation as well as all cases of convergent evolution. This, in turn, will
facilitate differentiation between ancestral and derived characters.
6 Brains of Insectivora
Based on paleontological studies on fossils, the Insectivora form geologically
the oldest eutherian group. In fact, many, if not all, recent orders of mammals
originated phylogenetic ally in insectivore-like ancestors (see Thenius 1969a, b,
1972; Thenius and Hofer 1960). Although recent forms exhibit a great variety
of evolved (apomorphic, derived, advanced) characters, they possess numerous
conservative (plesiomorphic, primitive, ancestral) traits which identify them as
the basic eutherian group. This is also true of the brain. The brain and nearly
all its components have been found to be smallest in certain groups of Insec
tivora compared with other mammalian orders. The most conservative species
of the extant Insectivora probably have undergone little evolutionary change
since their first appearance (permanent types). Hence, they can be expected to
be similar to the early forerunners of other mammalian orders, as e.g.,
Primates, and to represent a good reference base for evaluating brain evolution.
Therefore, in previous investigations (Andy, Baron, Bauchot, Frahm, Pirlot,
Stephan, since 1956), Insectivora (or subgroups of them) were used as the
reference base for brain comparisons with other orders (Scandentia, Chiroptera,
Primates, Macroscelidea).
Insectivora have not only retained a great number of primitive characters,
they also show an enormous variety of ecotypes. The Insectivora are in fact
more diverse anatomically than the members of any other order (Butler 1972).
Comparative study of insectivoran brain structure may therefore contribute to a
better understanding of the trends in brain evolution in relation to ecological
constraints.
The aims of this book are (1) to bring out major trends in brain evolution
among Insectivora and (2) to determine the extent to which brain structure and
composition relate to ecoethological considerations. This review does not, of
course, pretend to be complete in either its coverage of taxonomic and struc
tural diversity or in its treatment of the ecological and ethological facts. It
should, rather, be considered a first attempt to show how brain structure may
reflect an organism's ecological role and to gain some insight into the problem
of brain evolution.
In order to reflect the present state of knowledge about insectivoran brain
structure, the book also gives, in addition to many new data, a review of all
pertinent descriptive and experimental studies of which we were aware.
The raw data on brain structure volumes in a great number of tables are
presented in order (1) to make possible comparisons with similar data obtained
in other laboratories and from other taxonomic groups, (2) to encourage further
analysis with appropriate mathematical methods (e.g., multivariate analyses)
and (3) to stimulate further thought about possible interrelations with more and
new ecological and behavioral observations as knowledge in these fields
progresses.
Introduction 7
Acknowledgements
Thanks are due to many colleagues and friends in various parts of the world,
who helped to collect the material. Only some of them could be mentioned in
the key to the source of body and brain weight data given at the end of Table
5. For careful histological work, which was done in the Max-Planck-Institut fUr
Hirnforschung in Frankfurt, formerly Giessen, we are profoundly grateful to
Hermine Keiner, Clare Roberg, Monika Martin, Sigrid Wadle, Christina
Ronnacker and Anja Niehuis. Excellent assistance was given by Helga
Grobecker (photography), Hensy Rietveld-Fernandez (measurements), Michael
Stephan (computer programs and works), Volker Stephan (drawings and
graphics) and Helma Lehmann (secretarial work). Heartly thanks are due to
John Nelson for stimulating discussions and to Jessica Pottier for checking the
English text.
List of the Available Species
TENRECIDAE
TENRECINAE
Tenrec ecaudatus, Setifer setosus, Hemicentetes semispinosus,
Echinops telfairi
GEOGALINAE
Geogale aurita
ORYZORICTINAE
Oryzorictes talpoides, Microgale dobsoni, M. talazaci, Limnogale mergulus
POTAMOGALINAE
Potamogale velox, Micropotamogale lamottei, M. ruwenzorii
CHRYSOCHLORIDAE
Chrysochloris asiatica, C. stuhlmanni
SOLENODONTIDAE
Solenodon paradox us
ERINACEIDAE
ECHINOSORICINAE
Echinosorex gymnurus, Hylomys suillus
ERINACEINAE
Atelerix algirus, Erinaceus europaeus, Hemiechinus auritus
8 Brains of Insectivora
TALPIDAE
DESMANINAE
Desmana moschata, Galemys pyrenaicus
TALPINAE
Talpa europaea, T. micrura, Parascalops breweri, Scalopus aquaticus
SORICIDAE
SORICINAE
Sorex alpinus, S. araneus, S. cinereus, S. fumeus, S. minutus,
Microsorex hoyi, Neomys anomalus, N. fodiens, Blarina brevicauda,
Cryptotis parva, Anourosorex squamipes
CROCIDURINAE
Crocidura attenuata, C. flavescens, C. hildegardeae, C. jacksoni,
C. russula, C. suaveolens, Suncus etruscus, S. murinus, Scutisorex
somereni, Sylvisorex granti, S. megalura, Ruwenzorisorex suncoides,
Myosorex babaulti
Abbreviations
AA anterior amygdaloid area BA basal amygdaloid nucleus
AD nucleus anterodors. thalami BCI brachium colliculi inferioris
AM aqueductus mesencephali BH brain height
AMY amygdala BL brain length
ANT nuclei anteriores thalami BOL olfactory bulbs (MOB+AOB)
AOB bulbus olfact. accessorius BoW body weight
AP area postrema BrV brain volume
APT area pretectalis BrW brain weight
ARCH archicortex BW brain width
AS area striata
ASG area striata grey matter CAl capsula intema
AUD auditory nuclei CAM cortical amygdaloid nucleus
AvCg average of Crocidura-group CA 1 - areas of hippocampus
AvEr average of Erinaceinae CA4 retrocommissuralis
AvlF average of Insectivora CC corpus callosum
families and subfamilies CEA central amygdaloid nucleus
AvIS average of Insectivora species CER cerebellum
AvOr average of Oryzorictinae CGL corpus geniculatum laterale
AvPo average of Potamogalinae CGM corpus geniculatum mediale
AvSg average of Sylvisorex-group CHO chiasma opticum
AvSn average of Soricinae CLT nc!. centrolateralis thalami
AvTa average of Talpinae CM corpus mamillare
AvTn average of Tenrecinae CMT nc!. centromedialis thalami
AVT area ventralis tegmenti COA commissura anterior
COC commissura posterior
