Role of Inhibition for Temporal and Spatial Odor Representation in Olfactory Output Neurons: A Calcium Imaging Study

Abstract

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.

Olfaction in vector-host interactions

“…Although results emanating from these studies have expanded our knowledge about the neural mechanisms that shape the PN odour responses, it is important to acknowledge that these results may not directly transfer to the olfactory systems of other insects (reviewed by . A growing body of evidence, however, favours an interaction of interglomerular, or lateral, inhibitory connections between the processing channels in all insect species studied (Christensen et al 1998, Olsen and Wilson 2008, Sachse and Galizia 2002, Waldrop et al 1987. Lateral inhibition, through GABAergic LNs acting on both ORNs and PNs, is supported by ultrastructural analysis of their synaptic wiring (Boeckh and Tolbert 1993, Distler and Boeckh 1996, 1997a,b, Malun et al 1991a.…”

“…This in turn is believed to promote a more efficient neural code for odours that promote quality coding. In A. mellifera and M. sexta, however, physiological evidence supports a different model in which a substantial component of the lateral inhibition seems to act to sharpen the tuning curve of PNs rather than the ORN output, creating a more restricted spatial pattern of output from the odour-activated AL glomeruli (Christensen et al 1998, Sachse and Galizia 2002, Waldrop et al 1987. Evidence for a similar, but minor, component in D. melanogaster is available, but the functional implication of this arrangement is yet unknown (Olsen and Wilson 2008).…”

“…Disruption of lateral inhibition in the olfactory network through GABA receptor antagonists results in an overall increase in the output from the processing channels (Christensen et al 1998, Sachse and Galizia 2002, Wilson et al 2004. As a result, detection and discrimination thresholds are increased as evidenced by psychophysical data from A. mellifera and M. sexta indicating that the salient odour signal is lost (Hosler et al 2000, Mwilaria et al 2008.…”

Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis

“…GABA is a major inhibitory neurotransmitter in invertebrates (Kerkut et al, 1969;Usherwood, 1978), having an inhibitory effect at the neuromuscular junctions (Sattelle, 1992;Richmond and Jorgensen, 1999). GABA-mediated inhibition is thought to play a role in the processing of olfactory information both at the level of the antennal lobes (Christensen et al, 1998;Sachse and Galizia, 2002;Wilson and Laurent, 2005) and the mushroom bodies (Mizunami et al, 2005;Leitch and Laurent, 1996;Perez-Orive et al, 2002). GABA-immunoreactive neurons supplying terminal processes to the mushroom body calyces originate from dendrites situated either in the mushroom body lobes or in circumscribed regions of the lateral protocerebrum including the lateral horn (Homberg et al, 1987;Yamazaki et al, 1998;Bicker, 1999;Strausfeld and Li, 5 1999;Grünewald, 1999a).…”

Self-organization in the olfactory system: one shot odor recognition in insects

“…As a result, olfactory information seems to be encoded as combinatorial activation patterns of glomeruli in the AL [21,40,11,29]. In locust, these patterns are transformed to spatio-temporal patterns of active projection neurons (PNs) [22,25,50,24,39] which improve the separation of representations of similar odors [42,18,10]. The spatio-temporal code of the AL is transmitted to the mushroom body (MB) as discrete snapshots of activity [35].…”