Heinz Stephan

New and Revised Data on Volumes of Brain Structures in Insectivores and Primates

More than 2,000 data on volumetric measurements of 42 structures in a variety of up to 76 species (28 insectivores, 21 prosimians, 27 simians) are given. All volumes measured in serial sections were converted to fresh volumes of a brain having a standard size within a given species. The date are available to all scientists for comparison and analysis. To allow critical evaluation, details on fixation and preparation, on determination of fresh brain weights and volumes of brain parts and on intraspecific variability are given.

Gyrification in the Cerebral Cortex of Primates

The degree of cortical folding in primates has been analyzed using a gyrification index (GI). Correlation analyses of the GI with body weight, brain weight and neopallial volume show that the human data fit the general trend of the nonhuman anthropoids. Bigger primate brains exhibit a higher degree of fissurization, but a taxonomic difference that is independent of brain weight between prosimians and anthropoids has also been observed. In these regressions, anthropoids differed from prosimians by having a larger increase in gyrification for every unit increase in body or brain weight or neopallial volume. A stepwise regression also shows a prosimian-anthropoid difference. The best predictor for convolutedness in anthropoids is neocortical volume, while in prosimians it is brain weight. The GI in catarrhines is correlated with total sulcal length but not number of sulci. This result suggests paleontological studies of total sulcal length can give direct information on the evolution of cortical folding in primates.

QUANTITATIVE COMPARATIVE NEUROANATOMY OF PRIMATES: AN ATTEMPT AT A PHYLOGENETIC INTERPRETATION

All primates as well as many, if not all, recent orders of placental mammals have their phylogenetic origin in insectivorelike ancestors. This conclusion has been derived from paleontological studies on fossils. Although the brains of the early forerunners of mammals have not been preserved, clues to the shape of the brain and its surface pattern, to its size and to that of some of its individual subdivisions may be obtained from natural or artificial endocranial casts of fossil skulls. In this way, a direct study of the phylogenetic development of certain characteristics of the brain is possible. Edinger has brought this branch of scientific research, known as paleoneurology, to world-wide recognition. The amount of information that can be obtained from endocranial casts is necessarily restricted. Generally, statements concerning the finer structural details of the brain, especially those that are not represented on the surface, cannot be made. It would therefore be impossible to acquire any knowledge about the p h y b genetic development of such particulars without additionally employing the indirect method of comparing the brains of recent species now in existence. The results of this scientific approach, which is known as comparative neuroanatomy, can be used to a certain degree in the interpretation of phylogenetic relationships, if the comparisons are based on the insectivores. The recent representatives of the insectivores (to which comparative neuroanatomical investigations are necessarily restricted) are not uniform with regard to brain development. Using quantitative methods, we have tried (since 1956) to identify the species with the most primitive cerebral pattern. We have grouped together these primitive forms as “basal insectivores”.t To this group belong representatives of the tenrecs (Tenrecidae) , hedgehogs (Erinaceidae) and shrews (Soricidae) . The primitivity of the brains of the basal insectivores is reflected in the fact that all progressive structures

Evolutionary trends in limbic structures

and complexes of cerebral structures, respectively, are quantitatively the least developed. With regard to the quantitative composition of the brain, the basal insectivores represent a fairly uniform type. In contrast, the remainder of the insectivores reveal distinct marks of higher

Quantitative neuroanatomy of the brain of the La Plata dolphin, Pontoporia blainvillei

Structural differentiation and/or size of allocortical limbic structures (hippocampus, schizocortex, septum) are clearly more advanced in higher primates and man than in low (basal) Insectivora. In contrast, olfactory structures (olfactory bulb and olfactory cortices) are clearly smaller in higher Primates than in Insectivora. The opposite trends imply the existence of two functional systems in the allocortex (olfactory and limbic) being predominantly independent of one another. Within the hippocampus the greatest changes from Insectivora through Primates are found in area CA 1. The enlargement of CA 1 is clearly the highest within the hippocampus and its architectonic changes are striking. In the low Insectivora the CA 1 pyramidal layer is very dense and narrow. In Primates the pyramidal cells spread into the stratum oriens, and in man they are finally dispersed over the whole stratum and reach the alveus. In the schizocortex the enlargement of the entorhinal region is accompanied by structural differentiations which are reflected both in laminar and regional complexity.

Volume comparisons in the cerebellar complex of primates. II: Cerebellar nuclei

SummaryThe brain of the La Plata dolphin, Pontoporia blainvillei, was studied with methods of quantitative morphology. The volumes and the progression indices of the main brain structures were determined and compared with corresponding data of other Cetacea, Insectivora and Primates.In Pontoporia, encephalization and neocorticalization are clearly greater than in primitive (“basal”) Insectivora. The indices are in the lower part of the range for simian monkeys. The paleocortex is regressive in accordance with the total reduction of the olfactory bulb and olfactory tract. In contrast to the situation in primates, the septum, schizocortex and archicortex are not progressive in Pontoporia. The striatum and cerebellum are strongly progressive, corresponding to the efficiency and importance of the motor system in the three-dimensional habitat. The diencephalon, mesencephalon and medulla oblongata show considerable progression. Obviously, this is correlated with the extensive development of structures of the acoustic system.The superficial correspondence of the brains of dolphins and primates in relative size and in the degree of gyrencephaly is rather a rough morphological convergence than a sign of functional equivalence. It is coupled to a strongly divergent development of the various functional systems in the two mammalian orders according to their specific evolution.

Quantitative Cytoarchitectonics of the Cerebral Cortices of Several Prosimian Species

Volumes of medial, interposed, and lateral cerebellar nuclei (MCN, ICN, and LCN) were measured in Insectivora, Scandentia, and Primates, including man. The relative size of the nuclei was expressed in size indices. Insectivora had by far the smallest cerebellar nuclei. The simians, in general, had larger cerebellar nuclei than the prosimians, but there was considerable overlap. From Insectivora to man, the MCN was the least progressive and the LCN the most progressive. The indices are expected to reflect the relative size of the three longitudinal zones of the cerebellum (vermis/MCN, pars intermedius/ICN, hemisphere/LCN). They, together with those of the ventral pons and cerebellum (part I), are discussed in relation to the predominant locomotor pattern of a species, and with reference to evolutionary trends in primate phylogeny.

Größenänderungen im olfaktorischen und limbischen System während der phylogenetischen Entwicklung der Primaten

The classical architectonic studies represented by the works of Meynert (1872), Betz (1881), Campbell (1905), Elliot-Smith (1904, 1907), Vogt (1904, 1906, 1910), Vogt and Vogt (1907), Brodmann (1908, 1909), Economo and Koskinas (1925) and many others reached a “golden age” in the first decades of our century. These studies were based mainly on qualitative descriptions of structural forms, nerve cell morphology, and myelinization in different regions of the cortex. The investigations were mostly done on histological sections stained with Nissl-methods (cytoarchitectonic studies) and with methods demonstrating myelin (myeloarchitectonic studies). Important results were obtained, when (1) brains of many different mammalian species were compared (e.g., Brodmann, 1909) or (2) data from morphological and physiological studies were compared (e.g., Vogt and Vogt, 1907). Unfortunately these approaches were not followed by most later researchers, with the result that subjective and nonreproducible descriptions of minute morphological differences in the laminae or in cell structure increasingly prevailed. The discussions (1) about “haarscharfe Grenzen” (= boundaries fine as a hair) between brain regions, and (2) about the exact number of laminae in a given region of the cortex finally left the realm of science and were not even semantic problems. The consequence of this “development” was severe criticism of cytoarchitectonic studies (Lashley and Clark, 1946; Bailey and v. Bonin, 1951). Since that time workers using cytoarchitectonic methods have had to overcome a wall of more or less justified suspicion. A general suspicion about this type of brain research, however, is not justified, as the results of Hassler on the substantia nigra (1937) and the thalamic nuclei (1959) and the work of Stephan on the allocortex (1975) demonstrate. In these and other cases, the important traditions of classical investigations are apparent—the significance of the morphological structures are ascertained by comparisons among species and with the results of independent physiological studies. The mass of modern axonal transport and electrophysiological studies clearly show by the coincidence of architectonic and functional entities that cytoarchitectonic studies can be a useful tool in working out the function of a brain structure, as for instance, vertical structures such as ocular dominance columns (Hubel and Wiesel, 1963, 1977), barrel fields (Woolsey and Van der Loos, 1970), and dendritic bundles (Fleischhauer, 1974; Fleischhauer et al., 1972).

Vergleichend-anatomische Untersuchungen am Uncus bei Insectivoren und Primaten

Aussagen uber die phylogenetische Entwicklung einer Ordnung aufgrund vergleichendanatomischer Untersuchungen an rezenten Arten sind besonders dann gut fundiert, wenn Stadien aus ihrer generellen Entwicklungslinie rezent noch vorhanden sind. Fur die Primaten trifft dies voll zu. Sie stammen von Insektivoren ab (Remane 1961, u. a.) und die evolutive Stufenfolge — Insektivoren — Halbaffen — Affen — Menschenaffen — Mensch — ist relativ gut gesichert (Starck 1962). Die Insektivoren stellen somit eine gute Bezugsbasis fur die Beurteilung der evolutiven Fortschritte der Primaten dar. Besonders gilt dies fur die primitiven, wenig spezialisierten, rein terrestrischen Formen, die wir zur Gruppe der „basalen“ Insektivoren zusammengefast haben. Bezuglich des Gehirns zeichnen sie sich durch geringste Cortexgrose bei primitivster Cortexzusammensetzung aus. Hierzu gehoren Vertreter der Tenreciden, Soriciden und Erinaceiden. Im Gegensatz dazu zeigen andere Insektivoren, insbesondere die makroptischen Macroscelididen und die semiaqua-tilen Arten (aus verschiedenen Familien) bereits deutlich Merkmale einer Hoherentwicklung. Sie sind deswegen als Basalformen ungeeignet.

Phylogeny of the Primate Septum Telencephali

Publisher Summary The macromorphological changes in the archicortex, which in its rostro-ventral region eventually lead to the formation of the uncus, are examined in insectivores and primates. These animals are best suited for conclusions with regard to the progress of evolution toward man. The hippocampus descends even more into the depth, and the original orientation of its longitudinal axis, from dorso-rostra1 to ventro-caudal, undergoes a 90° turn. This is due to the expansion of the corpus callosum and the increasing development of the temporal lobe. In this process, the isocortex grows in a rostra1 direction, moving laterally along the allocortex. At the same time, the lateral isocortex expands ventral, and eventually, in its basal parts, also medial. If these two movements are applied to the caudal part of the hedgehog brain, the allocortex of the hedgehog assumes a developmental stage, which is very similar to the one present in higher primates. It shows then that a narrow strip of Ammonshorn forms the proximal part of the uncus, that is, the gyrus uncinatus. The band of the fascia dentata, which originally lies medial to the former, has assumed a caudal position and forms the limbus giacomini. Between them lies the anterior basal segment of the sulcus hippocampi. In many of the higher primates, and in man, a part of the hippocampus appears again at the distal end of the uncus; however, not with its superficial layer but with its deepest layer, that is, the alveus. This inverted hippocampus is called the gyrus intralimbicus and originates from a region that is also inverted in the hedgehog and lies next to the band of the fascia dentata, though still in a medial position, where it is covered by the brain stem.