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По стандарту ВАК Республики Беларусь: Sergei SAVELYEV, REGULARITIES OF VERTEBRAL BRAIN EVOLUTION [Электронный ресурс]: электрон. данные. - Минск: Белорусская цифровая библиотека LIBRARY.BY, 17 сентября 2021. - Режим доступа: https://library.by/portalus/modules/psychology/readme.php?subaction=showfull&id=1631881934&archive=&start_from=&ucat=& (свободный доступ). – Дата доступа: 20.01.2022.
Sergei SAVELYEV, REGULARITIES OF VERTEBRAL BRAIN EVOLUTION / Science in Russia, №2, 2011, C.22-30.
by Sergei SAVELYEV, Dr. Sc. (Biol.), Head of the Department of Embryology, RAMS Institute of Human Morphology
Why the structures emerging at some stage of biological evolution in the vertebrate brain are retained even many million years later in the progeny quite different from their distant predecessors? Why these formations did not reduce, did not disappear when they were seemingly no longer needed, as it should have taken place in accordance with the traditional concepts of historical development of living organisms? What is the basis of this conservatism?
Answers to these questions must be found. Let us discuss unique properties of the nervous system, distinguishing it from other systems. The phylogenetic changes underlying it are based on the multifunctional principle, introduced in 1875 in science by Anton Dorn, a German zoologist (foreign member of St. Petersburg Academy of Sciences from 1904). According to his concept, each organ is characterized by one main function and several secondary ones. The limbs of terrestrial mammals are usually offered as an example: the animals use them for movements on the ground, but at the same time capture the gain, use for swimming or defense. The first function is considered as an initial one, while other functions are supplementary. When the habitat changes, the main function can become additional and vice versa. This is the case with the limbs. For example, in deuterohydrous animals* the limbs which had been used for movement on the ground often transformed into flippers, till complete loss of the sustentacular function, like in modern cetaceans.
In the nervous system the multiple function principle is realized differently. The obvious example is evolution of the prosencephalon of birds. It emerged in ancient vertebrates as the center for analysis of olfactory signals and this main role was constantly perfecting. However, we face a paradox: though it is obvious that birds descended from ancient reptiles with a well-developed olfactory system, they have virtually lost a capacity to distant chemoreception, that is, they "lost" susceptibility to odors (except parrots, albatrosses, and some other groups).
By analogy with the limbs, it could be expected that the prosencephalon of birds would acquire new characteristics or be retained as a rudimentary organ. Moreover, it did not disappear as a structure, on the contrary, it was much larger than in modern reptiles. By the way, the histological findings indicate that all archaic struc-
* Life on the Earth started and developed in a water medium. Later on some representatives of terrestrial animal classes, which had originated from water ancestors, returned in the course of evolution to aqueous life (Phyllopoda class, whales, some turtles, snakes, etc.).--Ed.
Main stages of formation of the nervous system in the CHORDATA during the Cambrian (590-550 mln years ago). Arrows show the direction of evolutionary changes.
tures inherited by birds from reptiles have been not only retained, but also enlarged.
What are the causes of evolutionary conservatism of the bird prosencephalon structure? The links between neurons underlie the stability of the nervous system and make it unique. Each of them has a well-developed system of processes--dendrites and axons from several microns to several meters long. A total of 10,000-100,000 synaptic contacts, providing information exchange between the neurons and eventually between the brain compartments, including those located far from each other, are located on the surface of dendrites and axons and the neurons proper. This multiplicity of cell-to-cell interactions and the mechanisms of heterogeneous information flow processing make each nerve cell a multifunctional unit.
Let us emphasize that the neurons are universal and process the signals of any kind. It is important that these signals have a more or less resembling coding of impulses coming from the receptor system. Digressing we would like to mention here that this characteristic is already utilized by medicine for making a prosthetic hearing appliance, when open contacts from a special device are just inserted into the acoustic nuclei of the human metencephalon. After this operation the neurons adapt to unusual signals and the lost capacity is restored. The universal nature of the neurons allows to use virtually any brain compartment for information processing from compartments with a different specialization in case of change of the function. That is why almost complete loss of olfaction by birds did not lead, as we have mentioned above, to morphological losses in their prosencephalon. There developed a specialized associative center: the ancient olfactory center neurons started processing of signals coming from various organs of senses and motor systems. This evolutionary variant was so effective for birds that there was no need for new structures, such as the mammalian multilamellar neocortex*
* Neocortex--new regions of the cerebral cortex, just outlined in lower mammals and constituting a greater part of the cortex in humans.--Ed.
Origin of terrestrial vertebrates.
(discussed below). As a rule, the nervous system once formed, exists for a rather long time. This is the basic philosophy of its conservatism: changing the functions, a specialized compartment of the brain retains its morphological structure at the expense of intracerebral bonds. But the question is: for how long?
ON THE QUANTITY AND QUALITY
Let us discuss, for example, one of the amphibian mesencephalon structures--the tentum. It is mainly responsible for visual signal processing. The majority of Apoda, amphibians without limbs, inhabiting the soil and seemingly looking like earthworms, lost vision. However, one of them, Chtonerpeton viviparum, retained visual centers no worse than modern tailed amphibians (as our laboratory studies have shown), though the eyes are rudimentary and lie at a depth of the derma. It means that the unrequired compartment is structurally retained in the Apoda for over 250 mln years. Hence, the multifunctional nature of large structures of the brain virtually guarantees retention of traces of its archaic organization in modern animals.
These examples demonstrate the main method of evolutionary changes in the nervous system "construction". However, new structures do emerge in it for solution of unusual adaptive problems. This often takes place on the available base, but without its radical restructuring, like, say, in birds. The essence of a close in fact mode of phy-logenetic changes in the organs has been formulated by Nikolaus Kleinenberg, a German zoologist, long ago--in 1886. He suggested calling the phenomena in morphological evolution, when the organs are replaced by other ones, substitution. It was assumed that the formation of new organs involved the destruction of initial ones. Later on the founder of animal evolution morphology Academician (from 1920) Alexei Severtsov introduced a concept of substitution in homotopic and heterotopic location of a new organ. The former implied substitution of the disappearing organ by a new one with the same specialization, the latter meant emergence of a "substitute" in a different area of the body. But later on
Appearance and histological sections of the main structures of CHTONERPETON VIVARUM brain: a-prosencephalon hemispheres; b-mesencephalon, metencephalon, and prosencephalon; c-cerebellum and metencephalon; d, e-section through nasal conchas and an eye. Magnification shows a rudimentary eye in the derma under the cuticle.
it was found that these concepts just partially reflected the essence of the events in the nervous system. Substitution is always conjugated with reduction of the organ; but it is otherwise in the nervous system. Eventually, the initial nervous centers retain their morphological structure, though start performing somewhat different tasks. Adapting the above-mentioned phyloge-netic principle to evolution of the brain, we can say that it is realized in both homotopic and heterotopic variants, but without reduction of the initial structures. Later on we are going to discuss these regularities in the main groups of vertebrates.
The morphological evolution of the nervous system is important as an instrument extending the limits of adaptive potentialities. As a result, limitations of some behavioral reactions are cancelled and others are forming. This process continues till the emergence of the brain too much specialized for further restructuring. It should be pointed out that quantitative changes in the nervous system are much more rapid than qualitative ones. The former make up initial resources for structural adaptations of the nervous tissue. Qualitative morphological rearrangements are extremely difficult and usually require special conditions or long time. This difference is mediated by the special position of the brain and spinal cord in vertebrates.
Studies of amphibians, reptiles, and mammals have shown that 20-22 percent of quantitative changeability of the brain is standard for viable larvae or young animals born from the same couple of parents. The neurons were counted in the brain compartments and in the main peripheral analyzers. It was found out that the oldest structures (metencephalon and medulla oblongata) were characterized by 7-13 percent changeability, while evolutionarily new structures possessed 18-25 percent changeability. However, quantitative variability was fixed in virtually all compartments.
Individual changeability for anamnia (lower protohy-drous vertebrates--fishes, amphibians) varies from several thousands to tens of millions of neurons, for amniotes (higher vertebrates-reptiles, birds, mammals) it varies from hundreds of thousands to several billions. As each neuron has numerous contacts with other cells and can be a memory carrier, it is justified to expect an appreciable difference in the behavior of individuals even in the most homogeneous population. The relevant ethological validations are numerous and cover virtually all groups of vertebrates. This means that individuals solving certain problems better or worse than others exist in any population. If the biological situation is stable, nobody will make use of this difference.
If the environment is unstable, sex competition high, and food insufficient, the quantitative differences in the brain become significant. Moreover, they make up a decisive reserve if the behavioral reactions standard for the species are exhausted. And if their individualized form offers advantages for getting the food, it is then fixed by reproductive advantages, the probability of retention of the quantitative characteristics of the brain of this species is increasing. Probably this very mechanism underlies wide-scale adaptive changes in the brain of the majority of protohydrous vertebrates. Depending on their nutrition pattern and development of organs of senses, it differently increases in size, which is effective for solution of specific adaptive problems within the framework of the existing structure of the nervous system. Significant evolutionary events, leading to alteration of the habitat and emergence of new taxons, are associated with changes of a different kind.
It is clear that the formation of qualitatively new structures in the nervous system takes a long time and needs special conditions, for they should differ from the
Morphology of the amphibian and reptile brain; dorsal (a-d) and lateral (e, f) surfaces: a, e-crocodile; b-heccon; c-axolotle; d, f-frog.
traditional habitat and be attractive for vertebrates. This is guaranteed by abundant food and effective reproduction. If this biologically beneficial "niche" is retained for a long time, animals get a chance for acquiring a qualitatively new neuromorphological structure.
The emergence of ecological conditions of this kind was rare in the history of vertebrates. All these events were characterized by emergence of organisms with qualitatively new nervous system structures. The first of them was emergence of the Chordata presumably more than 550 mln years ago. It was rather accidental, but not a fatal evolutionary regularity. A group of small flat worms resembling turbellaria* still inhabited shallow water bodies with plenty of food. As filter feeders with a passive life style, they strived to live in maximally beneficial alimentary territories. Thus, they plunged the hind part of the body into bottom deposits (a similar "anchoring" was widely used by modern bottom-dwelling invertebrates). Remote effects of such simple adaptive actions of ancient worms were the formation of a dorsal (spinal) nerve cord and muscle chorda preventing its deformation. All ended in the fusion of segmental ganglia (nodules) of the dorsal nerve cord with subsequent formation of the central ventricle. This was paralleled by segregation of the ventral ganglia to the level of somatic ganglia. They formed the base for innervation of internal organs. Of course, the Chordata would not have emerged without specific transitional environment. Shallow water,
* Turbellaria are ciliary worms; live in seas, fresh water bodies, rarely on dry land and in the soil.--Ed.
Structure of the nervous system in amphibians shown for representatives of the orders: a-ARUNA, b-URODELA, c-APODA.
plenty of food, and conditions fit for reproduction guaranteed the flourishing of benthopelagic filter feeders. Subsequent evolution of the species took place under more diverse conditions and led to the emergence of numerous protohydrous vertebrates.
Other major qualitative changes in the brain of vertebrates are associated with their terrestrial life. This event led to significant morphological restructuring in the nervous system and other organs. There were formed limbs, pulmonary respiration, specialized integuments, and other signs, due to which the archaic tetrapodes started terrestrial life. Such wide-scale restructuring could not occur within a short period of time without a special transitional medium. Starting terrestrial life, the ancient amphibians developed a more perfect olfactory system, respiration control, and a complex of stem centers for limb control. The visual, acoustic, and vestibular systems have changed too.
Peculiar soil labyrinths or timber stocks of the Carboniferous* could serve as transitional between water and earth media. Under these conditions the animals used fins for swimming movements and for support. The skin respiration, gills, and rudimentary lungs functioned in parallel because of high humidity. The development of hydroaerial organs of senses and motor systems in the transitional medium justified biological advantages, due to which the vertebrates inhabited well protected territories with plenty of food. It seems that the environmental factors promoted gradual evolution of the nervous system in ancient amphibians, due to which the spinal centers and the red nucleus** for limb control, vomeronasal organ (additional olfactory organ for evaluation of odors in water and air, fixes the odors at a subconscious memory level), secondary acoustic and vestibular centers had probably emerged.
The third historical development period of the nervous system was formation of brain in archaic reptiles. It was in the reptiles that the associative compartment first formed in this organ. It "grew" from the mesencephalon and proved to be such a useful acquisition that for millions of years the reptiles became a predominating group of vertebrates. The associative center would have never formed without serious biological necessity, which emerged at the beginning of evolution of the reptiles as a method of adaptation to aggressive environment. They had to permanently compare the information delivered from different organs of senses and to make complex decisions because of rapidly changing situations. The protohydrous vertebrate brain had no abilities of this kind. They selected one of the instinctive forms of behavior for quite different reasons. A simple comparison of stimulation levels in the brain centers was sufficient for realization of one of the programs. The reptiles became the owners of an analytical device of an absolutely new type: it functioned on the basis of comparison of information received from each organ of senses. As a result, the signal contents, not the stimulation fact, played a key role.
In fact, the bases of associative principle to make decisions emerged in the reptiles. It is clear that we are speaking here about rudimentary signs of this characteristic of the brain, but it is important that they emerged in the reptiles. Perhaps the history of the reptiles comprises a much greater number of neurological experiments than we can imagine. Suffice it to mention just one more of their acquisitions, cortical structures of prosencephalon. The sex competition combined with unusual development of olfaction and the above-mentioned vomeronasal system formed the basis for their emergence. These structures stemmed from a new center providing integration of sex signals with other organs of senses and exhibiting activity only during reproduc-
* Carboniferous corresponds to the fifth period of the Paleozoic of geological history. It began 345 mln years ago and lasted for 65 mln years.--Ed.
** Red nucleus is one of the structures of mesencephalon, responsible for involuntary coordinated automatic movements of the limbs.--Ed.
Conditions of archaic reptile brain development.
tion. Apparently for its success the archaic reptiles had to make all body systems work for it and ignore everything else, even getting of food, during this period.
The associative and cortical centers of the reptile brain would not have emerged without rather peculiar conditions and rather long evolution in a specialized transitional medium. Of course, this ecological niche was not adapted for placid flourishing of a young group of vertebrates. Most likely, their neurological acquisitions resulted from adaptation to extremely intricate natural medium and aggressive competitive environment. During the Carboniferous, the plant trunks, where the archaic reptiles found abundant guaranteed food, could be quite fit for living. Their food presumably consisted of protohy-drous vertebrates, who had appeared there before and used it as a convenient place for habitation and reproduction. The reptiles living in such environment had to possess well-developed vestibular system and distant analyzers. The absence of light implied that their olfactory system had to be qualitatively different, as it had to serve as an important distant analyzer and as a regulator of sexual behavior. The evolved auditory system became more fit for orientation in darkness.
Over several tens of millions of years of stringent competition in the plant labyrinths, the reptiles developed a unique brain with a rather perfect set of neurological structures and an effective associative center. In the reproduction period, the entire brain was regulated by the new cortical structure in the prosencephalon wall. It became the specialized center regulating sexual behavior, which none of the vertebrates had had before. Hence, the brain of the vertebrates became a perfect system for solving the main biological problems of any type, survival and reproduction. With this behavioral resource the reptiles left their aggressive cradle and very rapidly became the predominating group on the planet.
Transition of archaic reptiles to habitation on trees was the key event for the beginning of mammalian brain evolution.
FROM BIRDS TO MAMMALS
The emergence of brain in birds cannot be regarded as an evolutionary event in principle, which is linked with qualitative restructuring of the brain. They themselves probably were to disappear soon after their emergence. It was a deadlock adaptive specialization, saved by previously described loss of olfaction. The archaic birds inherited its huge neurological substratum due to changes in food preferences. After they began to eat in shallow waters, they stopped using olfaction as a leading system of afferentation*. Vision became the main analyzing system, hearing--a supplementary one. To get food in water, the archaic birds** moved on their hind limbs, which gradually led to an appreciable reduction of load on fore-limbs and partial rudimentation of the hand.
Narrow specialization presupposed their rapid dying out, but transition to swimming and diving to get food led to development of wing-like fore-limbs (it was presumably at this evolutionary stage that penguins emerged, who never flied). Diving and swimming created physical conditions for the development of tubular bones, potent thoracic muscles, a system of pulmonary air sacs and plumage. Apparently necessity to get food in cold waters became one of the main stimuli to become warm-blooded. But wing-like swimming limbs were used not only for swimming. The ancient birds used them for peculiar "running over water", which became a transitional phase before active flight. Moreover, water as a transitional medium created necessary conditions for gradual accumulation of changes in the nervous sys-
* Afferentation is a constant flow of nerve impulses from organs of senses to the nervous system.--Ed.
** See: Ye. Kurochkin, "The Origin of Birds", Science in Russia, No. 2, 2009.--Ed.
tern, and hence, emergence of wings and transition to flying did not cause its radical restructuring.
And now a few words about mammals. They represent a rather strange group as regards their neurological status. The advantages of their brain developed from integration of sexual system functions. As we have mentioned above, the cortical structures of the reptile brain emerged as a result of the vomeronasal organ development. The mammals went much further. An associative center of quite a new type formed on the prosencephalon structure. It started regulating the work of already existing sensory systems. Autonomous mechanisms of the brain remained at the level of ancient centers, while all complex acquired functions developed in the prosencephalon cortex. In addition to olfaction and sexual integrative centers, the mammals are characterized by the development of the sensomotor system and mechanisms of the kinaesthetic (body) control. The cerebellum formed paired hemispheres only in these animals. Its sizes are so great, that its surface often exceeds neocortex sizes. Moreover, an appreciable (and sometimes greater) part of the neocortex provides somatic, sensomotor, and motor functions.
So strange a specialization can develop only under rather peculiar habitation conditions. The plant falls of the Carboniferous were a complex three-dimensional medium for reptiles, but their cerebellum failed to reach the level of this structure in birds. The mammals forming in the transitional medium had faced extremely high requirements to an analysis of the body position and coordination of movements. So stringent kinaesthetic regulation could form on the earth's surface only in tree branches. Apparently it was in tree crowns that the main sensomotor, olfactory, and acoustic advantages of the mammals had formed. The habitation conditions can be responsible for the emergence of the neocortex and development of somatic sensitivity, the development of which led to the emergence of receptor formations of the derma--the hair. Innervated by free nerve endings, they effectively increased the somatic sensitivity and then became the cause of development of the hair integument. It is noteworthy that subsequent utilization of hair for thermoregulation blurred their initial destination.
A quite new requirement to the nervous system first emerged in the tree crowns. Comparative analysis of information received from organs of senses was insufficient for archaic tree mammals. This mode of work of the associative systems precluded prediction of events, and this very capacity became decisive in getting food and for survival. Only flight could help the mammals escape these problems. However, only the Chiroptera order used it.
The main structural aftereffects of habitation in the tree crowns were the neocortex, two-hemisphere cerebellum, and capacity (though rather insignificant) to predict the development of events. This peculiarity of the mammals after their settlement on the soil and in water created appreciable behavioral advantages for them. The capacity to assess probable events became a key to their domination on the planet.
Thus, we can conclude: without long existence of a transitional medium there could be no sufficient time for variation of structural organization of the nervous system, as this system was too conservative for rapid and radical morphological transformations. The hypothesis on the important role of transitional media and understanding of specific features of the nervous system evolution proceeding from the modern level of knowledge will, we believe, shed new light on the causes of brain development in modern vertebrates and humans.