Glial patterns during early development of antennal lobes of Manduca sexta: A comparison between normal lobes and lobes deprived of antennal axons

Abstract

The synaptic neuropil of the olfactory (antennal) lobe of the moth Manduca sexta is subdivided into histologically conspicuous structures called glomeruli that are typical of olfactory systems in vertebrates and invertebrates. Each glomerulus consists of the highly branched neuritic arbors of both primary olfactory axons and antennal-lobe neurons, bounded by a nearly complete envelope of glial cells. We have studied events occurring during the first half of metamorphic adult development. The first signs of organization of the neuropil into glomeruli are changes in glial cells. Prior to the ingrowth of olfactory axons from the antenna, glial cells form a continuous border around the neuropil. When olfactory axons begin to reach the lobe, glial cells embark on a stereotyped series of changes: the border becomes disrupted, glial cells begin to proliferate and extend processes into the outer regions of the neuropil, and some glial cells migrate toward the center of the neuropil. Shortly thereafter, glomeruli emerge from the neuropil, delineated by glial cells. If, however, afferent axons are prevented from ever reaching the antennal lobe, glomeruli never develop and the glial cells remain almost entirely restricted to a thick layer bordering the neuropil. Thus sensory axons have a direct influence not only on neuronal but also on glial differentiation. Our results lead us to suggest that the glial cells may be in a position to act as intermediaries in developmental interactions between sensory axons and antennal-lobe neurons.

Development of depolarization‐induced calcium transients in insect glial cells is dependent on the presence of afferent axons

“…Migration of mouse cerebellar granule neurons has been shown to depend on intracellular calcium signaling mechanisms, and starts only after the functional expression of N-type VACCs Rakic, 1992, 1998). In Manduca, there is not only a very close temporal correlation between the development of voltage-dependent calcium transients and the migration of AL glial cells in normal ALs, but also an absence of both development of voltage-dependent calcium transients and glial migration in deafferented ALs (Oland and Tolbert, 1987). In addition, the variance of the [Ca 2ϩ ] i transients in late stage 5 glial cells was significantly larger than in earlier and later stages.…”

“…Metamorphosis is considered to start with the molt from larva to pupa and to end with the emergence of the adult moth. Metamorphic development can be divided into 18 stages, recognized by changes in structures that are visible through the pupal cuticle (Oland and Tolbert, 1987).…”

“…In addition, the amplitudes of the [Ca 2ϩ ] i transients increased by a factor of 15. Interestingly, it is at late stage 5 that glial cells start to migrate toward the center of the neuropil in the AL to surround developing glomeruli, the migration induced by formation of a glomerular template by the ingrowing olfactory receptor axons (Oland and Tolbert, 1987;Oland et al, 1990). Migration of mouse cerebellar granule neurons has been shown to depend on intracellular calcium signaling mechanisms, and starts only after the functional expression of N-type VACCs Rakic, 1992, 1998).…”

Development of a glial network in the olfactory nerve: role of calcium and neuronal activity

“…Manduca sexta (Lepidoptera: Sphingidae) were reared in the departmental insect-rearing facility under a long-day photoperiod as described previously (Oland and Tolbert, 1987). Metamorphic development starts with pupation and ends with the emergence of the moth after passing through 18 stages, each lasting about a day.…”

“…Metamorphic development starts with pupation and ends with the emergence of the moth after passing through 18 stages, each lasting about a day. Pupae were staged by following changes of structures that are visible under the pupal cuticle (Oland and Tolbert, 1987). Before dissection of the brain, pupae were anesthetized by cooling on ice or by exposure to CO 2 for at least 30 min.…”