The Antennal Lobe Spreads Activity Across The Projection Neuron Population

Several hypotheses have been proposed for the role of the first olfactory relay (antennal lobe or olfactory bulb). One poses that it serves to sharpen the odor tuning of individual principal neurons, via lateral inhibition between like-tuned glomerular units (Mori and Shepherd 1994). Another suggests that it serves as a faithful relay of representations by olfactory afferent neurons (Wang et al. 2003). I propose that, with the exception of special odors (e.g., some phero-mones), the antennal lobe spreads afferent activity across its component neurons to optimize the use of coding space. The system would act as a "mixing box." Information is not lost; rather it is distributed broadly across the population, in a step critical to the formation of synthetic representations by postsynaptic neurons (presented in Figures 10.4-10.7).

Early Olfactory Circuits in Insects (Figure 10.2a)

Olfactory sensory neurons at the base of sensilla converge on glomeruli where they contact projection neurons (uniglomerular in Drosophila, multiglomerular in locusts). Projection neurons then send an axon to protocerebral structures (mushroom bodies and/or lateral horn).

Projection Neurons in Glomerulus DM2 Are More Broadly Tuned than Their Afferents (Figure 10.2b)

Exploiting Drosophila genetics and olfactory receptor physiology by J. Carlson, it is possible to characterize the tuning of olfactory sensory neurons whose glomerular projections are known (Or22a here). Using patch-clamp recordings, the projection neurons projecting to DM2 are then sought and characterized under the same conditions. Both olfactory sensory neurons and projection neurons were tested with the same 34 odors at pairs of histograms compare their tunings within two consecutive 100 ms long bins. Note that DM2 tuning of the projection neurons is considerably broader than that of their olfactory sensory neurons' input. If projection neurons are more broadly tuned than the receptor neurons to which they are presumably directly connected, since they share the same glomerulus, information must be distributed across the antennal lobe through local circuits.

The Redistribution of Activity across Projection Neurons Can Be Interpreted as Enabling a Better Use of Coding Space (Figure 10.2c)

A system of tightly tuned projection neurons that recapitulate or sharpen olfactory sensory neurons' tuning diminishes the chances of projection neuron coactivation and would thus concentrate coding to the volume around its main dimensions (that is, the glomerular preferences). A system of broadly tuned projection neurons, by contrast, spreads representations in the coding space defined by the projection neuron population. If average projection neuron response probability is close to 50%, as we observe, the use of projection neuron coding space is possibly optimal.

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