Myelination of the developing lateral olfactory tract and anterior commissure

Abstract

Both the lateral olfactory tract (LOT) and anterior limb of the anterior commissure (AC) carry olfactory information. The LOT forms the projection from the olfactory bulb to the ipsilateral olfactory cortices, while the AC carries odor information across the midline to the contralateral olfactory cortex and bulb. The LOT and AC differ on a number of dimensions, including early development and functional onset. The present work, examining their myelination in mice, reveals additional important differences. For example, the LOT initiates myelination 3-4 days earlier than the AC, evidenced by both an earlier increase in myelin basic protein staining seen with immunohistochemistry and an earlier appearance of myelinated fibers using electron microscopy. While both exhibit a period of rapid myelination, it occurs 4-5 days earlier in the LOT than the AC. The tracts also respond differently to early sensory restriction. Unilateral naris occlusion from the day after birth to postnatal day 30 had no consistent effects on the AC but resulted in significantly thinner myelin sheaths relative to axon caliber in the LOT. Finally, the two tracts differ structurally (the LOT contains larger, more densely packed axons with significantly thicker myelin sheaths resulting in a conduction velocity that is more than twice as fast as the AC). The findings indicate that these two large, accessible tracts provide an important means for studying brain maturation due to basic differences in both the timing of their maturation and general organization.

The mouse olfactory peduncle 4: Development of synapses, perineuronal nets, and capillaries

“…Interestingly, within the plexiform layer of the AON, these parameters did not change over the developmental period examined, indicating that synapse maturity is achieved earlier than P5. Such early maturation within Layer 1 would allow the necessary neural activity for other developmental processes, such as early myelination (Collins & Brunjes, ), and is consistent with similar findings from the rat piriform cortex demonstrating early synaptic development (Westrum, ). Finally, EM analysis also confirmed extensive neuropil expansion throughout the period examined.…”

“…Axons first enter the AC much later (E16; Silver, Lorenz, Wahlsten, & Coughlin, ). A similar pattern is seen in the onset and rapid phase of myelination in the two tracts: the LOT undergoes myelination between postnatal Day (P) 9–13, but the process does not occur in the AC until P11‐14 (Collins & Brunjes, ). Considerable volumetric growth occurs in AONpP from postnatal Days P10–P20, with reduced expansion from P20 to P30; similar changes are found in the growth in dendrites of its pyramidal cells (Brown & Brunjes, ; Brunjes, Collins, Osterberg, & Phillips, ; Brunjes & Kenerson, ).…”

“…Differences in the timing of maturation between the LOT and AC are mirrored in functional differences within the olfactory pathway (Collins & Brunjes, ). As mentioned above, the LOT arises early in order to allow olfactory function at birth.…”

“…Four ages were selected for study: P5 (early in olfactory system development), P13 and P17, (ages which coincide with the period of rapid myelination of the AC; Collins & Brunjes, 2018), and P30 (when OB growth plateaus; Hinds & Hinds, 1976). At least three animals were examined per age.…”

“…ALAC, anterior limb of the anterior commissure; AONpP, anterior olfactory nucleus pars principalis; LOT, lateral olfactory tract; SVZ, subventricular zone both glutamatergic (VGlut1 and VGlut2) and GABAergic (VGAT) synapses was examined in postnatal Day (P) 5-30 mice with immunofluorescence. A second set of quantitative electron microscopic studies examined synapses in P5, P11, P13, and mature function in the interhemispheric pathway (Collins & Brunjes, 2018). Because little is known about these crossed projections, a third set of studies characterized both the development of axons from pPl to the contralateral AONpP (Illig & Eudy, 2009) and the synapses formed by the projection.…”