When does a ganglion become a brain? Evolutionary origin of the central nervous system

Abstract

A brain, a neural structure located in the head, differs from a ganglion by the following characteristics: (1) a brain subserves the entire body, not just restricted segments; (2) it has functionally specialized parts; (3) it is bilobar; (4) commissures and neurons form the surface with axons in the central core; (5) interneurons are more numerous than primary motor or primary sensory neurons; and (6) multisynaptic rather than monosynaptic circuits predominate. A "cephalic ganglion" does not exist in any living animal and probably never occurred even in extinct ancestral species. It also is not a developmental stage in the ontogenesis of any vertebrate. Amphioxus may represent an intermediate stage in the evolution of the vertebrate nervous system, but the anatomic relationship between the notochord and neural tube is more complex. The decussating interneuron of amphioxus, to mediate a primitive coiling reflex away from any stimulus, provides a phylogenetic explanation for the pattern of crossed long ascending and descending pathways in the subsequent evolution of the vertebrate central nervous system. The evolution of the vertebrate central nervous system may have begun with free-living flatworms (planaria) that evolved before the divergence of metazoans into invertebrate and chordate branches. The planarian is the simplest animal to develop a body plan of bilateral symmetry and axes of growth with gradients of genetic expression, enabling cephalization, dorsal and ventral surfaces, medial and lateral regions, and an aggregate of neural cells in the head that form a bilobed brain. Neurons of the planarian brain more closely resemble those of vertebrates than those of advanced invertebrates, exhibiting typical vertebrate features of multipolar shape, dendritic spines with synaptic boutons, a single axon, expression of vertebrate-like neural proteins, and relatively slow spontaneously generated electrical activity. The planarian is thus not only the first animal to possess a brain, but may be the ancestor of the vertebrate brain.