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Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons

Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons
Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons
Inhibitory local interneurons (LNs) play a critical role in shaping the output of olfactory glomeruli in both the olfactory bulb of vertebrates and the antennal lobe of insects and other invertebrates. In order to examine how the complex geometry of LNs may affect signaling in the antennal lobe, we constructed detailed multi-compartmental models of single LNs from the sphinx moth, Manduca sexta, using morphometric data from confocal-microscopic images. Simulations clearly revealed a directionality in LNs that impeded the propagation of injected currents from the sub-micron-diameter glomerular dendrites toward the much larger-diameter integrating segment (IS) in the coarse neuropil. Furthermore, the addition of randomly-firing synapses distributed across the LN dendrites (simulating the noisy baseline activity of afferent input recorded from LNs in the odor-free state) led to a significant depolarization of the LN. Thus the background activity typically recorded from LNs in vivo could influence synaptic integration and spike transformation in LNs through voltage-dependent mechanisms. Other model manipulations showed that active currents inserted into the IS can help synchronize the activation of inhibitory synapses in glomeruli across the antennal lobe. These data, therefore, support experimental findings suggesting that spiking inhibitory LNs can operate as multifunctional units under different ambient odor conditions. At low odor intensities, (i.e. subthreshold for IS spiking), they participate in local, mostly intra-glomerular processing. When activated by elevated odor concentrations, however, the same neurons will fire overshooting action potentials, resulting in the spread of inhibition more globally across the antennal lobe. Modulation of the passive and active properties of LNs may, therefore, be a deciding factor in defining the multi-glomerular representations of odors in the brain.
glomeruli, olfaction, odor processing, modulation, synaptic integration
0303-2647
143-153
Christensen, Thomas A.
27febdf0-c3e2-4b26-940c-c52e62d07418
D'Alessandro, Giampaolo
bad097e1-9506-4b6e-aa56-3e67a526e83b
Lega, Joceline
6542b32a-7591-4359-aa8f-b2d0b085ff78
Hildebrand, John G.
d353421a-1786-4fa3-8e5a-ab0d6a665f49
Christensen, Thomas A.
27febdf0-c3e2-4b26-940c-c52e62d07418
D'Alessandro, Giampaolo
bad097e1-9506-4b6e-aa56-3e67a526e83b
Lega, Joceline
6542b32a-7591-4359-aa8f-b2d0b085ff78
Hildebrand, John G.
d353421a-1786-4fa3-8e5a-ab0d6a665f49

Christensen, Thomas A., D'Alessandro, Giampaolo, Lega, Joceline and Hildebrand, John G. (2001) Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons. Biosystems, 61 (2-3), 143-153. (doi:10.1016/S0303-2647(01)00163-0).

Record type: Article

Abstract

Inhibitory local interneurons (LNs) play a critical role in shaping the output of olfactory glomeruli in both the olfactory bulb of vertebrates and the antennal lobe of insects and other invertebrates. In order to examine how the complex geometry of LNs may affect signaling in the antennal lobe, we constructed detailed multi-compartmental models of single LNs from the sphinx moth, Manduca sexta, using morphometric data from confocal-microscopic images. Simulations clearly revealed a directionality in LNs that impeded the propagation of injected currents from the sub-micron-diameter glomerular dendrites toward the much larger-diameter integrating segment (IS) in the coarse neuropil. Furthermore, the addition of randomly-firing synapses distributed across the LN dendrites (simulating the noisy baseline activity of afferent input recorded from LNs in the odor-free state) led to a significant depolarization of the LN. Thus the background activity typically recorded from LNs in vivo could influence synaptic integration and spike transformation in LNs through voltage-dependent mechanisms. Other model manipulations showed that active currents inserted into the IS can help synchronize the activation of inhibitory synapses in glomeruli across the antennal lobe. These data, therefore, support experimental findings suggesting that spiking inhibitory LNs can operate as multifunctional units under different ambient odor conditions. At low odor intensities, (i.e. subthreshold for IS spiking), they participate in local, mostly intra-glomerular processing. When activated by elevated odor concentrations, however, the same neurons will fire overshooting action potentials, resulting in the spread of inhibition more globally across the antennal lobe. Modulation of the passive and active properties of LNs may, therefore, be a deciding factor in defining the multi-glomerular representations of odors in the brain.

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More information

Published date: 2001
Keywords: glomeruli, olfaction, odor processing, modulation, synaptic integration

Identifiers

Local EPrints ID: 29303
URI: http://eprints.soton.ac.uk/id/eprint/29303
ISSN: 0303-2647
PURE UUID: 00b40784-25a7-4c11-85de-5fc54a96e101
ORCID for Giampaolo D'Alessandro: ORCID iD orcid.org/0000-0001-9166-9356

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Date deposited: 12 May 2006
Last modified: 16 Mar 2024 02:48

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Contributors

Author: Thomas A. Christensen
Author: Joceline Lega
Author: John G. Hildebrand

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