Myron S. Jacobs

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

We review the evidence for the concept of the “initial” or prototype brain. We outline four possible modes of brain evolution suggested by our new findings on the evolutionary status of the dolphin brain. The four modes involve various forms of deviation from and conformity to the hypothesized initial brain type. These include examples of conservative evolution, progressive evolution, and combinations of the two in which features of one or the other become dominant. The four types of neocortical organization in extant mammals may be the result of selective pressures on sensory/motor systems resulting in divergent patterns of brain phylogenesis. A modular “modification/multiplication” hypothesis is proposed as a mechanism of neocortical evolution in eutherians. Representative models of the initial ancestral group of mammals include not only extant basal Insectivora but also Chiroptera; we have found that dolphins and large whales have also retained many features of the archetypal or initial brain. This group evolved from the initial mammalian stock and returned to the aquatic environment some 50 million years ago. This unique experiment of nature shows the effects of radical changes in environment on brain-body adaptations and specializations. Although the dolphin brain has certain quantitative characteristics of the evolutionary changes seen in the higher terrestrial mammals, it has also retained many of the conservative structural features of the initial brain. Its neocortical organization is accordingly different, largely in a quantitative sense, from that of terrestrial models of the initial brain such as the hedgehog.

Ultrastructure of the blood-brain barrier in the dolphin (Stenella coeruleoalba)

Light and electron microscopic methods were used for investigation of angioarchitectonics, glioarchitectonics and the structural basis of the blood-brain barrier in the dolphin Stenella coeruleoalba. It was shown that the cortical plate of the dolphin brain is extremely rich in capillaries and small arteries that are organized into a complicated net of continuous loops surrounding neuronal groups. The density of the capillary loops is related to the cytoarchitectural density of the cortex. It was also found that the neuronal microenvironment in the dolphin cortex is characterized by the presence of a large number of the astroglia-like cells that make a multi-layered investment surrounding capillaries and small arteries. These glial cells, unlike typical astrocytes of terrestrial mammals, have a large number of different organelles and their nuclei are similar to those of the oligocytes. The ultrastructure of the blood-brain barrier in the dolphin is characterized by the presence of extremely long tight junctions between endothelial cells and by specialized junctions between pericapillary astroglia-like cells. A belt of the glial end-feet interlocked with different types of junctions such as zonulae adherentes, maculae adherentes and gap junctions was found around all investigated capillaries. This system of specialized interendothelial and glio-glial junctions is tentatively hypothesized to be a feature of adaptation of the dolphin to the aquatic environment.

Comparative and Evolutionary Anatomy of the Visual Cortex of the Dolphin

The cetaceans (great whales, dolphins, and porpoises) are known to have descended back to the sea more than 50 million years ago and thus are considered as secondary aquatic mammals (Kesarev et al., 1977a,b; Gaskin, 1982; Gingerich et al., 1983). They completely adapted themselves to the new conditions, not only in terms of changes in body shape, but also in the structure and function of their neuromuscular apparatus and internal organs and, especially, in regard to development of the brain. They appear to have preserved characteristic features of the original structure of the brain of primitive mammals in far greater measure than have more advanced land animals. At the same time the cetaceans were in a position in this new environment to develop specific features of adaptation not characteristic of land mammals. Thus, studies of the cetacean brain structure may make it possible to move closer to unraveling some important problems of evolution of the mammalian brain. Genetically related to terrestrial mammals, whales are of particular evolutionary value and uniqueness since they have adapted themselves to activity in an aqueous medium according to laws characteristic of this Order alone and, in so doing, have made evident the potential possibilities of the structural adaptations of the brain and, in particular, the great adaptability of the cerebral cortex (Nikitenko, 1965; Tomilin, 1968; Ladygina and Supin, 1974; Zvorykin, 1963, 1977; Kesarev et al., 1977a; Mehedlidze, 1984; Morgane et al., 1986a,b).

Regional and cellular differences in rat brain protein synthesis in vivo and in slices during development

We compared the rate of protein synthesis in immature and adult rat brain In vivo to that in brain slices. After the incorporation of a flooding dose of [14C]valine, In vivo and in brain slices, the label in proteins was measured in CNS regions and in neuron‐ and glia‐enriched fractions. In regions In vivo in the adult, incorporation rates in corpus callosum were lower than in other regions, which were similar: in the young, cerebellum showed the highest rates and hypothalamus and cord the lowest. Since hypothalamus and cord were low in the young, there was no change during development in these two areas; in other areas incorporation rates in young were 2–3 times higher than in adult brain proteins. Incorporation rates in slices were lower than In vivo. In the young, cerebellum, olfactory bulb, and cord were close to In vivo, and other areas in slices from young incorporated at 60–90% of In vivo rates. In adult slices incorporation was 5–15% of that In vivo except in olfactory bulb, where it was 30%. In the cellular fractions, incorporation In vivo in young was close in the neuronal and glial fractions; in adults incorporation rates in neurons were higher, as the decrease in development was less in neurons than astrocytes. In slices in young, astrocytes incorporated amino acids at 100% of the In vivo rates, neurons at 60%; in adult slices, incorporation was at only 4–7% of the In vivo rate.

Rates of protein synthesis in brain and other organs

We previously found a decrease in protein synthesis in brain during development, which was much greater as measured in brain slices than in brain in vivo. In the present work such changes in brain were compared to those in other organs. With measurement of incorporation of flooding doses of [14C]valine into proteins of organs, the highest synthesis rate in the adult animal in vivo was found in liver (2.2%) followed by kidney (1.8%), spleen (1.6%), lung (1.0%), heart (0.7%), brain (0.6%) and muscle (0.5%). In immature animals the synthesis rate was highest in spleen (2.6%) followed by liver (2.4%), kidney (1.7%), lung (1.6%), brain (1.5%), heart (1.1%), and muscle (0.9%). Protein synthesis in slices from each tissue proceeded at lower rates than in vivo, especially in adults. The tissue affected the most by the preparation of the slices was muscle.

Some Comparative Aspects of Auditory Brainstem Cytoarchitecture in Echolocating Mammals: Speculations on the Morphological Basis of Time-Domain Signal Processing

A number of studies have described the gross morphology and general hypertrophy of the auditory brainstem nuclei in Cetacea and Chiroptera (See Henson, 1970 for review; Zvorykin, 1959, 1963). However, there have been only a few attempts to describe the cytoarchitecture of the auditory brainstem in detail (Osen & Jansen, 1965; Schweizer, 1981; Zook & Casseday, 1982) or to make comparisons of brainstem auditory cytoarchitecture between echolocating species of bats and marine mammals. We will begin here to take a closer look at the auditory brainstem of a number of microchiropteran and odontocete cetacean species, initially focusing upon a few distinctive cytoarchitectonic patterns found in three cell groups: the anteroventral cochlear nucleus (AVCN), the medial nucleus of the trapezoid body (MNTB) and the ventral nucleus of the lateral lemniscus (VNLL). In some species of bat and dolphin, cells in these nuclei form orderly rows or columns that are more uniformly aligned than is found in most nonecholocating mammals. In the two dolphin species examined, rows of cells perpendicular or at an angle to the fibers of the trapezoid body are present in the caudal part of the AVCN and in the MNTB. Within the VNLL in some bat species there is a distinctive alignment of cell soma, in columns rather than rows, parallel to fiber bundles.

Amino acid incorporation in relation to molecular weight of proteins in young and adult brain

Rates of protein synthesis were studied in immature and adult rat brain tissue. After an amino acid incorporation period, in vivo or in incubated slices from brain, the soluble protein was fractionated according to molecular weight by column chromatography. In examining soluble whole proteins, no direct correlation between molecular weights and synthesis rates could be established; the highest synthesis rates were found in fractions around 70,000 MW and below 10,000. Incorporation into the subunits after fractionation by SDS gel electrophoresis was proportional to subunit molecular weight, with rates of incorporation into the largest subunits being the highest. The results suggest a relationship between turnover rate and structure of subunits of brain proteins.

Rates of protein synthesis—a review

The rates of protein synthesis can be measured by a variety of methods including pulse labeling, massive precursor administration, Scornik method, continuous feeding of labeled precursor, infusion, and pellet implantation. Each technique has some advantages and disadvantages. Massive precursor administration and infusion are the most widely used. The advantage of massive precursor administration is its simplicity, however, the amino acid concentration used is much higher than physiological levels. Infusion, however, is much more complicated as a technique and requires complicated calculations. The synthesis rates can also be calculated from degradation curves. Some of the above techniques can be used both in vivo and in vitro, and also for different organs (Shahbazian et al. (1987), Int. J. Dev. Neurosci., 5: 39-42). The brain has rapid rates of protein synthesis both in vivo and in vitro, the latter being much lower for adults.

Histologic monitoring of murine mammary tumor lysis induced by an autologous serum factor.

Abstract An autotumorolytic factor (SFIII), derived from a serum fraction of mammary tumor-bearing mice, has been demonstrated to be active when injected into the donor mouse. Gross and histologic assessment of tumors was made at 3, 12, 24, 48, 72, and 96 hr postinjection of SFIII. Concomitantly, lymph node, spleen, liver, kidney, thymus, and lung tissues were examined in these treated tumor animals and compared to non-tumor-bearing animals and a single animal exhibiting spontaneous tumor breakdown. Tumor destruction began at 3 hr postinjection with interlobular connective tissue breakdown accompanied by hemorrhage. Infiltration of connective tissue, where still present, by lymphocytes, plasma cells, and macrophages progressively increased with time. Lysis of tumor tissue subsequently spread to intralobular epithelium resulting in large cavitations containing fragmented tissue and debris, characterized by coagulative and liquefactive necrosis and caseation. Lymphoid tissues showed no significant immune reactivity. This pattern of induced tumorolysis appeared to have been duplicated in spontaneous tumor breakdown. Liver, lung, kidney, and the normal mammary tissue were apparently unaffected by the tumorolytic factor.