Activity blockade does not prevent the construction of olfactory glomeruli in the mothManduca sexta

Abstract

During metamorphic development, the arrival at the olfactory (antennal) lobe of olfactory receptor axons initiates the process of glomerulus formation. The glomeruli are discrete spheroidal regions of neuropil that are the sites of synaptic interactions among receptor neurons and their target antennal-lobe neurons. The process of glomerulus formation begins as groups of receptor axons form protoglomeruli. These dense clusters of terminal branches mostly are discrete entities from the time they can be recognized, although a few branches from neighboring protoglomeruli overlap laterally. A previous study by Schweitzer et al. [Schweitzer E. S., Sanes J. R. and Hildebrand J. G. (1976) Ontogeny of electroantennogram responses in the moth, Manduca sexta. J. Insect Physiol. 22, 955-960] has shown that odor-induced activity in the receptor neurons can be detected first in recordings from the axons in the antennal nerve only in the last few days of metamorphic development and thus could not influence the process of glomerulus formation. In this study, we have tested directly the possibility that an earlier presence of spontaneous activity in either the receptor axons or the antennal-lobe neurons could affect the process. Tetrodotoxin, a Na(+)-channel blocker, was injected into the hemolymph prior to the onset of glomerulus formation to block any spontaneous Na(+)-dependent activity. Subsequent intracellular recordings from antennal-lobe neurons revealed no spike activity. Comparison with vehicle-injected control animals at stages during and after glomerulus formation revealed no differences in the localization of receptor-axon terminal branches in the glomeruli, in the border of glial cells that forms around each glomerulus, or in the morphology of the tufted glomerular arbors of one of the antennal-lobe neurons. We conclude that: (1) the process of glomerulus formation is largely independent of activity; and (2) glomeruli as modular units of the CNS more closely resemble cortical barrels than cortical columns, both in their ontogeny and in the lack of an obvious effect of activity on the morphology of the neurons arborizing within them.

Multiple factors shape development of olfactory glomeruli: Insights from an insect model system

“…1 (C,D)] . Even as they begin to form, the protoglomeruli each occupy an almost discrete territory with little overlap of laterally extending axonal branches (Oland et al, 1996b). Within a stage, however, the individual protoglomeruli become Distinguishing processes as axonal or dendritic is even less straightforward in the invertebrates than it is in the vertebrates.…”

“…In the moth, odorant-induced activity in the receptor neurons first appears only in the last few days of metamorphic development, long after glomeruli develop (Schweitzer et al, 1976); and intracellular recordings from multiglomerular neurons revealed no responses to electrical stimulation of the antennal nerve prior to stage 9 (Tolbert et al, 1983). However, some of the receptor axons and some of the antennal-lobe neurons are spontaneously active during the critical stages of glomerulus formation (Oland et al, 1996b; H. G. Marrero and L. A. Oland, unpub.…”

Activity-dependent modulation of neural circuit synaptic connectivity

“…The dogma has long been that invertebrate circuits are hard-wired from the early stages of development, and do not employ activity-dependent refinement in a manner comparable to vertebrates. Indeed, a strong body of experimental evidence supports this position, in both primary sensory circuits and higher order systems (Berdnik et al, 2006; Hiesinger et al, 2006; Jefferis et al, 2004; Oland et al, 1996; Scott et al, 2003; Srahna et al, 2006). However, both classical and recent evidence has shown that environmental experience in invertebrates is capable of modulating the connectivity of sensory and higher order circuits (Chiba et al, 1988; Devaud et al, 2001, 2003; Fahrbach et al, 1995; Sachse et al, 2007; Withers et al, 1993).…”

Plateau Potentials in Developing Antennal-Lobe Neurons of the Moth,Manduca sexta

“…Developing neurons in primary olfactory centers [antennal lobes (ALs)] of the brain of the sphinx moth, Manduca sexta, show bursts of electrical activity (Mercer and Hildebrand 2002a;Oland et al 1996). Here, we examine intrinsic properties that contribute to the characteristic form of electrical activity apparent in these developing neurons: their ability to generate prolonged membrane depolarizations or plateau potentials.…”

“…During metamorphosis, including critical stages of glomerulus formation, electrical activity can be detected in antennal nerve (sensory afferent) fibers and in AL neurons of the moth (Mercer and Hildebrand 2002a;Oland et al 1996). In AL neurons, this activity is characterized by prolonged membrane depolarizations that resemble plateau potentials (Mercer and Hildebrand 2002a).…”