Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons
Introduction
Olfactory glomeruli, the dense knots of synaptic neuropil that characterize early olfactory centers in diverse organisms, are believed to play a key role in the recognition and discrimination of odors (Schild and Riedel, 1992, Hildebrand and Shepherd, 1997, Christensen and White, 2000), but the details of their involvement is unclear. Little is known, for example, about the cellular and synaptic mechanisms underlying inter-glomerular communication and how these interactions help create a unique neural representation of each olfactory stimulus in the brain. Insect glomeruli are interconnected by a diverse network of multi-branched, GABAergic local interneurons (LNs; Fig. 1A) (Christensen et al., 1993, Leitch and Laurent, 1996). Unlike the periglomerular and granule cells in the olfactory bulb of mammals and other vertebrates (Shipley and Ennis, 1996), insect LNs branch profusely, and many extend processes into every glomerulus in the first-order processing center, the antennal lobe (Fig. 1B). Networks of LNs provide the major source of inhibitory input to projection neurons (PNs), and these connections are thought to serve a major function in shaping the multiglomerular patterns of activity evoked by olfactory stimuli (review: Christensen and White, 2000). Their characteristic wide-field organization suggests that LNs may function by distributing their inhibitory influence throughout the antennal lobe, thus globally modulating the output of the entire glomerular array (Fig. 1A, B). At present, however, there is no experimental evidence to support this general function.
Intracellular recordings from identified LNs in moths revealed that even in the absence of odor, LNs exhibit a steady level of background activity resulting from the convergence of axons from many olfactory receptor neurons (Christensen et al., 1993). When stimulated with odor, LNs respond with both graded synaptic potentials and action potentials (Fig. 1C). Furthermore, action potentials of more than one amplitude have been observed in many LNs (Matsumoto and Hildebrand, 1981, Christensen et al., 1993), suggesting the possible existence of active dendritic properties and dendritic spikes intermingled with larger overshooting spikes generated in the IS more proximally to the soma (Shen et al., 1999) (Fig. 1C). Thus it is possible that LNs participate in both local interactions with neurons in the same glomerulus that receives the sensory input, as well as more global interactions with neurons in neighboring glomeruli in the antennal lobe. In order to begin to address these issues, we examined the passive electrical properties of LNs using multi-compartmental models based on morphometric and electrophysiological data from identified LNs in the antennal lobe of the moth Manduca sexta.
Section snippets
Preparation for LN staining
Manduca sexta (Lepidoptera: Sphingidae) were reared on artificial diet under a long-day photoperiod (17-h light:7-h dark). All animals were used within 3–5 days following adult emergence, and the experimental procedures to access the brain have been detailed previously (Christensen et al., 1998). Lucifer Yellow CH was used to stain impaled neurons via intracellular electrodes for subsequent confocal microscopy (King et al., 2000). Neurons were stained by passing hyperpolarizing direct current
Results
In order to simulate a depolarizing potential propagating from glomeruli on one side of the antennal lobe to glomeruli on the other, we applied a voltage clamp in the IS at a point in the coarse, non-synaptic neuropil region of the LN (clamp C in Fig. 2B). The traces in Fig. 2C show that the membrane voltage at different points in the dendritic tree follows a similar time course, and this is confirmed by the compact attenogram to the left of the traces. As expected, attenograms revealed that
Discussion
Detailed compartmental models of LNs in the olfactory system of Manduca sexta are beginning to reveal important insights into the functional roles of inhibition in regulating glomerular activity at the earliest stage of odor-information processing in the brain. In the absence of anatomical data, while it is possible to make predictions about the attenuation of signals propagating through a dendrite, accurate morphometric data of the type we present here allows one to calculate the magnitude of
Acknowledgements
We are very grateful to Dr Ted Carnevale and Dr Al Scott for many helpful discussions and valuable advice, and to Jason Lashbrook and Brandon Williams for technical assistance. Supported in part by NIH/NIDCD grant DC02751 (JGH).
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