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Genetic Mechanisms of the Early Development of the Telencephalon, a Unique Segment of the Vertebrate Central Nervous System, as Reflecting Its Emergence and Evolution

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Abstract

The emergence of the telencephalon as a forebrain part with a complex structure is one of the most important aromorphoses in vertebrate evolution. The telencephalon developed and improved in evolution to allow higher nervous activity forms observed in animals and humans. A telencephalic anlage is separated at the earliest stages of vertebrate ontogenesis, when the anterior part of the neural tube differentiates into three cerebral vesicles: the prozencephalon as an anlage of the future forebrain, the mesencephalon as the future midbrain, and the rhombencephalon as the future hindbrain. The forebrain further differentiates to form the telencephalon and the diencephalon. The development of brain structures and regions is modulated by the expression of certain regulatory genes, which code for transcription factors and signaling molecules. Problems of the evolutionary origin and ontogenesis of the telencephalon are still poorly understood at the molecular level, although they are among central problems of modern developmental biology. Recent studies of the evolutionary mechanisms responsible for the emergence of the telencephalon in vertebrates have paid much attention to cyclostomes (lampreys and hagfishes) as the most evolutionarily ancient vertebrate groups and Tunicata (ascidians) and Cephalochordata (lancelets) as the closest relatives of vertebrates. Cyclostomes are of particular interest because they were the first in evolution to have the telencephalon as a separate morphological structure and because they might preserve the expression patterns and regulatory mechanisms characteristic of vertebrate ancestors. The review summarizes and analyzes the data accumulated in recent years from studies of the genetic mechanisms of early telencephalon development in lower vertebrates and searches for telencephalon homologs in two vertebrate-related chordate groups, Cephalochordata and Tunicata.

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Funding

The reported study and manuscript preparation were funded by the Russian Foundation for Basic Research, project no. 19-14-50215.

Experiments to study FoxG1 and Noggin in lampreys were supported by the Russian Foundation for Basic Research (project no. 18-04-00015). Analysis of Hh expression was supported by the Russian Science Foundation (project no. 19-14-00098). Experiments to functionally study the anterior head genes in clawed frog were supported by the Russian Foundation for Basic Research (project no. 18-29-07014). Studies of the Anf gene were supported by the program “Basic Research for Biomedical Technologies” of the Russian Academy of Sciences.

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  1. Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    A. V. Bayramov, G. V. Ermakova & A. G. Zaraisky

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  1. A. V. Bayramov
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  2. G. V. Ermakova
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  3. A. G. Zaraisky
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Correspondence to A. V. Bayramov.

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Translated by T. Tkacheva

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Bayramov, A.V., Ermakova, G.V. & Zaraisky, A.G. Genetic Mechanisms of the Early Development of the Telencephalon, a Unique Segment of the Vertebrate Central Nervous System, as Reflecting Its Emergence and Evolution. Russ J Dev Biol 51, 162–175 (2020). https://doi.org/10.1134/S1062360420030054

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