Brain Evolution and Comparative Neuroanatomy

The central nervous system has changed over the course of time independently in different lineages of animals. The broad array of variation in nervous system structure reflects the diversity of successful niches and lifestyles available in the biological world. Various parts of the central nervous system have been elaborated in some invertebrate taxa, particularly in some arthropods and molluscs, as well as in various vertebrate taxa. Among the latter, elaboration of the forebrain is arguably the greatest in birds and mammals, both of which also exhibit highly cognitive behaviors. The distribution of elaborated brains across phylogeny demonstrates that evolution has not occurred in a simple, unilinear ‘progressive’ manner from simple to complex but rather independently in different lineages, resulting in a diversity of morphology such that both simpler and more complex nervous systems may be adaptive, depending upon the existing selective pressures. Key concepts Rostrocaudally organized nervous systems are present in all bilaterally symmetrical animals, and the patterning (homeobox) genes that specify them were established at the origin of this radiation. Among invertebrates, elaborated (enlarged and/or increased in complexity) central nervous systems have independently evolved multiple times, particularly within the arthropod lineage, which includes insects, and in some molluscs, including octopus. In vertebrates, there is a wide range of the degree of elaboration of the central nervous system, but the same major divisions of the brain are present in all taxa: the forebrain (prosencephalon) consisting of the telencephalon and diencephalon, the midbrain (mesencephalon), and the hindbrain (rhombencephalon), consisting of the metencephalon and myelencephalon. The cranial nerves of vertebrates number up to 25, depending on the taxon. They consist of some purely motor, some purely sensory, and other mixed nerves that have both motor and sensory components. Olfactory and the related vomeronasal and terminal nerves are present in the forebrain; the oculomotor and trochlear nerves arise in the midbrain and the rest arise and/or come into the hindbrain. At the transition from invertebrate chordate to the first vertebrates, it is likely, based on fossil evidence, that the first steps involved the gain of paired eyes and the elaboration, at least to a modest extent, of the diencephalon, along with the gain of branchial bars and a muscularized pharynx for predatory feeding. This was rapidly followed by the elaboration of neural crest and neurogenic placodal tissues for the gain of the peripheral nervous system, the dermal skull, and a host of additional tissues. The vertebrate brain is relatively conservative in the components of the hindbrain and midbrain, although some instances of extreme variation occur in these regions. The forebrain exhibits extensive variation in its degree of elaboration, and both lesser and greater elaborated forebrains can be adaptive, depending upon the existing selective pressures. In the vertebrate telencephalon, the nonlimbic (nonhippocampal and nonolfactory) pallial areas are relatively unelaborated in lampreys, some sharks, some bony fishes, and in amphibians but, in contrast, are highly elaborated in hagfishes, other sharks and in skates and rays, many bony fishes, and in amniotes – reptiles, birds, and mammals. The telencephalic pallium is arguably the most elaborate in birds and mammals. Across vertebrates, ascending sensory systems have two basic patterns. One involves a predominantly direct projection of sensory axons to the dorsal thalamus, referred to as lemnothalamic, and subsequent relay to the telencephalic pallium. The other predominantly involves a less direct input to the dorsal thalamus (or to more posterior diencephalic relay nuclei in some fishes) via the roof of the midbrain, referred to as collothalamic, and subsequent relay to other pallial areas. The variation in lifestyle, i.e. the niche, of different species is reflected in specializations in brain features. Both simpler and more complex nervous systems can be adaptive. Specializations can occur in the sensory and motor periphery as well as anywhere along the entire length of the neuraxis and in the dorsal versus parts of it as well. Among the specializations is the extreme degree of pallial elaboration in both birds and mammals. Likewise, birds and mammals share many other features including the highest brain-body ratios and multiple behavioural abilities, including remarkably high levels of cognitive ability. They likewise may share high levels of consciousness, and comparative studies of their neural features may contribute to the quest to identify the neural basis for consciousness and how it is produced. Keywords: forebrain; alar plate; cranial nerves; lamination; thalamus