Two types of somatic spines provide sites for intercellular signaling during calyx of Held growth and maturation

Dendritic spines have been described in developing and mature systems, but similar extensions from cell bodies are less studied. We utilized electron microscopy image volumes, uniquely collected across a range of early postnatal and month-old mice, to characterize and describe two types of somatic processes that extended into and under the developing calyx of Held (CH), which we named type 1 and type 2 spines. Type 1 spines occurred singly, were mostly vermiform in shape, and formed regularly spaced indentations into the CH. Type 1 spines appeared in concert with the earliest expansion of the CH by P3, peaked at P6 and returned to low density at P30. Type 2 spines were intertwined into a secondary structure called a spine mat, which has not previously been described in the CNS, and were more complex geometrically. Type 2 spines formed after the CH crossed a size threshold, reached maximum density at P9, and were absent from most CHs at P30. Both spine types, but a higher density of type 1 spines, were sites for synapse formation. Spine mats brought pre- and postsynaptic neurons and glial cells into contact, and were captured in stages of partial detachment and engulfment by the presynaptic terminal, suggesting trans-endocytosis as a mode of removal ahead of maturity. In conglomerate, these observations reveal somatic spines to be sites for chemical neurotransmission and chemical sampling among synaptic partners and glia as tissue structure transforms into mature neural circuits.