Expression of synaptic proteins and development of dendritic spines in fetal and postnatal neocortex of the pig, the European wild boar Sus scrofa

Synapse formation is a critical step in neuronal development. Current knowledge is largely based on altricial rodents where synapse formation and maturation proceed largely postnatally. In precocially born mammals such as guinea pig presynapse and spine formation start well before birth. Here, we analysed the developmental expression of proteins associated with synapse formation and maturation together with the development of basal dendritic spines of pyramidal neurons of visual and somatosensory cortex of the pig, an emerging translational model for human neurodegenerative disorders. A total of 23 selected proteins was quantified with Western blots. Most were detectable from midgestation embryonal day (E) 65 onwards. About half reached the adult expression level seen in postnatal day (P) 90 pig cortex already two weeks before birth (gestation 114 days) in somatosensory, albeit not yet in visual cortex. For instance, major molecular components of synaptic plasticity such as GluN2B, CamKIIα, α-actinin-2, synaptopodin and T286 phosphorylated CamKIIα were expressed at E100 in somatosensory cortex. Dendritic spine type quantification with DiI-labeled material revealed an increase of total dendritic protrusion from E70 onwards. The increase was steepest in somatosensory cortex which had, at E110, a proportion of mushroom spines equal to the proportion present at P90. Together, matching the ungulate life history, a rapid development of functional synaptic connectivity in prenatal somatosensory cortex serves the somatomotor abilities essentially required by the newborn nest-fledgling. Results support the “cascading” model of a sequential maturation of cortical areas, and in precocial species the cascade starts well before birth.