Evolution and development of interhemispheric connections in the vertebrate forebrain

Abstract

Axonal connections between the left and right sides of the brain are crucial for bilateral integration of lateralized sensory, motor, and associative functions. Throughout vertebrate species, forebrain commissures share a conserved developmental plan, a similar position relative to each other within the brain and similar patterns of connectivity. However, major events in the evolution of the vertebrate brain, such as the expansion of the telencephalon in tetrapods and the origin of the six-layered isocortex in mammals, resulted in the emergence and diversification of new commissural routes. These new interhemispheric connections include the pallial commissure, which appeared in the ancestors of tetrapods and connects the left and right sides of the medial pallium (hippocampus in mammals), and the corpus callosum, which is exclusive to eutherian (placental) mammals and connects both isocortical hemispheres. A comparative analysis of commissural systems in vertebrates reveals that the emergence of new commissural routes may have involved co-option of developmental mechanisms and anatomical substrates of preexistent commissural pathways. One of the embryonic regions of interest for studying these processes is the commissural plate, a portion of the early telencephalic midline that provides molecular specification and a cellular scaffold for the development of commissural axons. Further investigations into these embryonic processes in carefully selected species will provide insights not only into the mechanisms driving commissural evolution, but also regarding more general biological problems such as the role of developmental plasticity in evolutionary change.

Subset of early radial glial progenitors that contribute to the development of callosal neurons is absent from avian brain

“…Sauropsids lack a homologous structure to the corpus callosum (21). In addition, the number of upper-layer-like cortical homologous neurons is reduced.…”

“…One of the most characteristic features of mammalian supragranular neurons is the projection of contralateral efferences through the corpus callosum. Sauropsid brains lack a homologous dorsal pallial interhemispheric tract, and it is possible that the appearance of delayed progenitors committed to the generation of novel interhemispheric connections emerged as a functional advantage through positive selection (21). This appearance could be a major cause of brain divergence in the evolutionary roots of the eutherian branch of mammals.…”

“…The appearance of neurons with callosal projections in the upper layers is considered an important event in the evolution of the mammalian neocortex, as there is no corpus callosum in sauropsid brains (21). Based on selected gene expression patterns, Suzuki et al suggested that upper-layer-like cortical neurons are situated in a different sector of chick pallium with respect to the position of lower-layer-like neurons (22).…”

Anatomia microcirúrgica da região do sulco limitante inferior da ínsula

“…Estudos experimentais neuroanatômicos em macacos rhesus mostraram que essa comissura interconecta a parte mais rostral (ou uncal) do corno de Ammon do hipocampo e giros denteados associados, e suas fibras também passam do pré-subiculum até o córtex entorrinal contralateral (Nieuwenhuys et al, 2008;Suarez et al, 2014).…”

“…Essa estrutura interconecta o epitálamo bilateralmente, e é composta por algumas fibras que, ascendendo com a stria medullaris thalami, decussam na comissura habenular e terminam no complexo habenular de substância cinzenta contralateral (Nieuwenhuys et al, 2008). A comissura das habênulas também contêm axônios originários do bulbo olfatório e pallium medial que terminam contralateralmente em alvos paliais, subpaliais e diencefálicos (Suarez et al, 2014).…”