Sachse, Silke and C. Giovanni Galizia. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87: 1106J Neurophysiol 87: -1117J Neurophysiol 87: , 2002 10.1152/jn.00325.2001. The primary olfactory brain center, the antennal lobe (AL) in insects or the olfactory bulb in vertebrates, is a notable example of a neural network for sensory processing. While physiological properties of the input, the olfactory receptor neurons, have become clearer, the operation of the network itself remains cryptic. Therefore we measured spatio-temporal odor-response patterns in the output neurons of the olfactory glomeruli using optical imaging in the honeybee Apis mellifera. We mapped these responses to identified glomeruli, which are the structural and functional units of the AL. Each odor evoked a complex spatio-temporal activity pattern of excited and inhibited glomeruli. These properties were odor-and glomerulus-specific and were conserved across individuals. We compared the spatial pattern of excited glomeruli to previously published signals, which derived mainly from the receptor neurons, and found that they appeared more confined, showing that inhibitory connections enhance the contrast between glomeruli in the AL. To investigate the underlying mechanisms, we applied GABA and the GABA-receptor antagonist picrotoxin (PTX). The results show the presence of two separate inhibitory networks: one is GABAergic and modulates overall AL activity, the other is PTX-insensitive and glomerulus-specific. Inhibitory connections of the latter network selectively inhibit glomeruli with overlapping response profiles, in a way akin to "lateral" inhibition in other sensory systems. Selectively inhibited glomeruli need not be spatial neighbors. The net result is a globally modulated, contrast-enhanced and predictable representation of odors in the olfactory output neurons.

Co.rre1 atcon betvveen panems 1n c a Rd d. r = 0.92 (P < 0.001). B, Time courses of calcium• signals at selected glomeruli {dlfferern experinienl) a, Odours .elicit specific s1gnals upon s tiffUJiat•Oi1 (bar). b. Hexaoollcads to successive activat•on of dif.erent regions (see Inset) 2 8 5

Our findings offer novel insights into how a command chemical orchestrates an innate behavior by stepwise recruitment of central peptidergic ensembles.

Odours are represented by speci®c ensembles of activated glomeruli in a combinatorial manner within the olfactory bulb of vertebrates or the antennal lobe (AL) of insects. Here, we optically measured glomerular calcium activities in vivo in the honeybee Apis mellifera during olfactory stimulation with 36 pure chemicals differing systematically in carbon chain length (C-5±10) and functional group (aldehyde, ketone, alcohol, carboxylic acid and alkane). We show their glomerular representations in 38 morphologically identi®ed glomeruli out of the honeybee's 160. We measured the molecular receptive range of identi®ed glomeruli averaging up to 21 individuals. Of the 38 glomeruli measured, 23 show maximal activity in a speci®c range of chain length. Glomeruli preferentially responding to a functional group are also always broadly tuned to particular chain lengths. Furthermore, glomeruli with similar response spectra are often direct neighbours. The results allow conclusions about the interactions between olfactory receptors and odour molecules, and about the AL network.

A striking commonality across insects and vertebrates is the recurring presence of parallel olfactory subsystems, suggesting that such an organization has a highly adaptive value. Conceptually, two different categories of parallel systems must be distinguished. In one, specific sensory organs or processing streams analyze different chemical stimuli (segregate parallel systems). In the other, similar odor stimuli are processed but analyzed with respect to different features (dual parallel systems). Insects offer many examples for both categories. For example, segregate parallel systems for different chemical stimuli are realized in specialized neuronal streams for processing sex pheromones and CO(2). Dual parallel streams related to similar or overlapping odor stimuli are prominent in Hymenoptera. Here, a clear separation of sensory tracts to higher-order brain centers is present despite no apparent differences regarding the classes or categories of olfactory stimuli being processed. In this paper, we review the situation across insect species and offer hypotheses for the function and evolution of parallel olfactory systems.