Interactions among neurons and glial cells help to shape functional assemblies of neurons in the developing nervous system. We are studying neuron-neuron and neuron-glia interactions that lead to the formation of neuropil compartments, the olfactory glomeruli, in a tractable model system, the antennal lobe of the brain of the moth Manduca sexta. In previous years, we have shown that afferent axons induce the formation of glomerular branching patterns in neurons of the antennal lobe, and that this inductive influence requires the presence of glial cells. We hypothesized that olfactory receptor axons exert at least part of their influence by using the glial cells as intermediaries - in other words, that the receptor axons lay down a template, around which the glial cells build a scaffold, and subsequent neurite growth by antennal-lobe neurons is constrained to the template by the glial scaffold. We recently have discovered that the protoglomerular template laid down by the axons dissolves almost immediately in glia-deficient antennal lobes. Thus, we now plan to ask: (Specific Aim I) How do olfactory receptor axons establish the pattern of protoglomeruli? when and in what ways does this pattern deviate in the absence of sufficient numbers of glial cells? We also have found recently that members of one class of neuron, the uniglomerular projection neurons of the antennal lobe (similar in some ways to the mitral/tufted cells of the vertebrate olfactory bulb), interact much earlier with the incoming receptor axons than do other classes of neurons that we have studied in the past. Moreover, these projection neurons form a single glomerulus-like structure at the point where glomerulus formation ordinarily is initiated, even if sensory axons are prevented from growing in and inducing glomeruli. To elucidate the level of autonomy of the sensory axons and/or antennal-lobe glial cells in glomerulus development, we will ask: (Specific Aim 2) what roles does this class of CNS neuron play in glomerulus development? In addition, we will use heterotopic grafting tests to ask: (Specific Aim 3) How specific are the interactions between receptor owns and CNS neuronal and glial cells in developing glomeruli? Using the experimentally favorable insect nervous system, we will be able to do experiments not as readily performed in vertebrates. Answers to the questions we have posed should provide important insights into the cellular and molecular bases for the roles of afferent axons and glial cells in shaping subunits or compartments within the developing brain.

National Institute of Health (NIH)
National Institute of Neurological Disorders and Stroke (NINDS)
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Neurology B Subcommittee 2 (NEUB)
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Leblanc, Gabrielle G
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University of Arizona
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Goriely, Anita R; Secomb, Timothy W; Tolbert, Leslie P (2002) Effect of the glial envelope on extracellular K(+) diffusion in olfactory glomeruli. J Neurophysiol 87:1712-22
Dubuque, S H; Schachtner, J; Nighorn, A J et al. (2001) Immunolocalization of synaptotagmin for the study of synapses in the developing antennal lobe of Manduca sexta. J Comp Neurol 441:277-87
Wegerhoff, R; Rossler, W; Higgins, M et al. (2001) Fenvalerate treatment affects development of olfactory glomeruli in Manduca sexta. J Comp Neurol 430:533-41
Rossler, W; Oland, L A; Higgins, M R et al. (1999) Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J Neurosci 19:9865-77
Oland, L A; Tolbert, L P (1998) Glomerulus development in the absence of a set of mitral-like neurons in the insect olfactory lobe. J Neurobiol 36:41-52
Oland, L A; Tolbert, L P (1996) Multiple factors shape development of olfactory glomeruli: insights from an insect model system. J Neurobiol 30:92-109
Tolbert, L P; Sun, X J; Hildebrand, J G (1996) Combining laser scanning confocal microscopy and electron microscopy in studies of the insect nervous system. J Neurosci Methods 69:25-32
Willis, M A; Butler, M A; Tolbert, L P (1995) Normal glomerular organization of the antennal lobes is not necessary for odor-modulated flight in female moths. J Comp Physiol A 176:205-16
Krull, C E; Morton, D B; Faissner, A et al. (1994) Spatiotemporal pattern of expression of tenascin-like molecules in a developing insect olfactory system. J Neurobiol 25:515-34
Malun, D; Oland, L A; Tolbert, L P (1994) Uniglomerular projection neurons participate in early development of olfactory glomeruli in the moth Manduca sexta. J Comp Neurol 350:1-22

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