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The Journal of Neuroscience, December 8, 2004, 24(49):11108-11119; doi:10.1523/JNEUROSCI.3677-04.2004

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Behavioral/Systems/Cognitive
Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe

Hong Lei, Thomas A. Christensen, and John G. Hildebrand

Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson, Arizona 85721

In the insect antennal lobe, odor discrimination depends on the ability of the brain to read neural activity patterns across arrays of uniquely identifiable olfactory glomeruli. Less is understood about the complex temporal dynamics and interglomerular interactions that underlie these spatial patterns. Using neural-ensemble recording, we show that the evoked firing patterns within and between groups of glomeruli are odor dependent and organized in both space and time. Simultaneous recordings from up to 15 units per ensemble were obtained from four zones of glomerular neuropil in response to four classes of odorants: pheromones, monoterpenoids, aromatics, and aliphatics. Each odor class evoked a different pattern of excitation and inhibition across recording zones. The excitatory response field for each class was spatially defined, but inhibitory activity was spread across the antennal lobe, reflecting a center-surround organization. Some chemically related odorants were not easily distinguished by their spatial patterns, but each odorant evoked transient synchronous firing across a uniquely different subset of ensemble units. Examination of 535 cell pairs revealed a strong relationship between their recording positions, temporal correlations, and similarity of odor response profiles. These findings provide the first definitive support for a nested architecture in the insect olfactory system that uses both spatial and temporal coordination of firing to encode chemosensory signals. The spatial extent of the representation is defined by a stereotyped focus of glomerular activity for each odorant class, whereas the transient temporal correlations embedded within the ensemble provide a second coding dimension that can facilitate discrimination between chemically similar volatiles.

Key words: odor discrimination; ensemble recording; glomerulus; olfaction; spatiotemporal coding; synchrony

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Received Sep 6, 2004; revised October 21, 2004; accepted October 30, 2004.

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