Abstract
The conserved brain design that primates inherited from early mammals differs from the variable adult brain size and species-specific brain dominances observed across mammals. This variability relies on the emergence of specialized cerebral cortical regions and sub-compartments, triggering an increase in brain size, areal interconnectivity and histological complexity that ultimately lies on the activation of developmental programs. Structural placental features are not well correlated with brain enlargement; however, several endocrine pathways could be tuned with the activation of neuronal progenitors in the proliferative neocortical compartments. In this article, we reviewed some mechanisms of eutherians maternal–fetal unit interactions associated with brain development and evolution. We propose a hypothesis of brain evolution where proliferative compartments in primates become activated by “non-classical” endocrine placental signals participating in different steps of corticogenesis. Changes in the inner placental structure, along with placenta endocrine stimuli over the cortical proliferative activity would allow mammalian brain enlargement with a concomitant shorter gestation span, as an evolutionary strategy to escape from parent-offspring conflict.
Highlights
Placenta and brain are not recent innovations in vertebrate phylogeny (Aboitiz and Montiel, 2007; Renfree et al, 2013)
We propose a hypothesis of brain evolution where proliferative compartments in primates become activated by “non-classical” endocrine placental signals participating in different steps of corticogenesis
In an attempt to integrate evolutionary, developmental, and genomic data, we discuss (1) the evolutionary origin of mammals, (2) the comparative morphology of placenta, (3) neocortical development, (4) placenta–brain endocrine interactions, (5) potential molecular placenta–brain interactions extracted from transcriptome databases, and (6) we speculate about a hypothesis for the neocortical expansion observed in mammalian evolution that integrates in situ and neighboring cues with the control based on endocrine signals from placenta, from which some represent new pathways that should be explored further
Summary
Placenta and brain are not recent innovations in vertebrate phylogeny (Aboitiz and Montiel, 2007; Renfree et al, 2013). The acquisition of a large brain size in mammalian evolution (Rowe et al, 2011) is mainly explained by the activation of developmental programs that allow a radial and tangential laminar expansion of the cerebral cortical surface (Cheung et al, 2007, 2010; Aboitiz and Montiel, 2012; Molnár and Clowry, 2012) These events are correlated with the activation, and functional specialization of cortical proliferative compartments, named ventricular zone (VZ) and subventricular zone (SVZ; Kriegstein et al, 2006; Molnár et al, 2006; Cheung et al, 2007, 2010; Molnár, 2011; Aboitiz and Montiel, 2012). In an attempt to integrate evolutionary, developmental, and genomic data, we discuss (1) the evolutionary origin of mammals, (2) the comparative morphology of placenta, (3) neocortical development, (4) placenta–brain endocrine interactions, (5) potential molecular placenta–brain interactions extracted from transcriptome databases, and (6) we speculate about a hypothesis for the neocortical expansion observed in mammalian evolution that integrates in situ and neighboring cues with the control based on endocrine signals from placenta, from which some represent new pathways that should be explored further
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