Odor Coding in Projection Neurons of the Honeybee Brain

Abstract

Olfactory stimuli are coded by a spatio-temporal pattern of activity at the primary level of sensory integration, the olfactory bulb in vertebrates and the antennal lobe (AL) in insects (Hildebrand and Shepherd, 1997; Galizia and Menzel, 2000), indicating that multiple glomeruli encode particular chemical compounds as well as odor mixtures. A glomerular activity pattern may be translated into a cross-fiber-activity pattern in relay neurons (projection neurons, PN) enriched by temporal components, e.g. synchrony effects of spike activity (Laurent, 2003). In all studied insects, the inner antennocerebral tract (in honeybees, the median antennocerebral tract, mACT), connects the mushroom body (MB) and the lateral horn (LH) with the AL. Similarly, axons of the outer antenno-cerebral tract (in bees, the lateral ACT, l-ACT) innervates the LH and MB but in a reverse sequence: first the LH and then the lip region of the MB calyces. A third bundle of axons, called the mediolateral ACT, also innervates the LH and larger parts of the LH, but not the calyces. This third bundle of PNs will not be dealt with here. In the bee, the anatomy of the PN tracts is rather simple. The PNs of the m- and l-ACT receive input only from single glomeruli in the AL (uniglomerular PNs; Abel et al., 2001). Thus, the MB receives olfactory information only via uniglomerular PNs. Considering the similar anatomical features of the m- and the l-ACT neurons, we asked: (i) how do they terminate in the lip region of the MB calyx; (ii) how do these neurons differ in their olfactory response properties; and (iii) how is the activity pattern of these neurons translated into activity patterns at their outputs. We reconstructed >130 intracellularly marked PNs, aiming to analyse axon terminal patterns in the lip region of the MB. PN axons innervate large parts of the MB lips and terminate with up to 12 blebs per PN axon within the dendritic area of one Kenyon cell (KC) (Muller et al., 2002). These axon terminals provide overlapping inputs to KC dendritic areas. The blebs are not evenly distributed, accumulating in some regions of the lip and leaving others empty. Such an organization will lead to different combinations of inputs to the same KC dendritic areas. Since the dendritic branches of neighboring KCs overlap considerably, different PNs still terminate at many different KCs. However, clusters of KCs should receive similar combinations. Axon terminals of m- and l-ACT neurons appear to fully overlap in the lip regions of the calyces, making it likely that a given KC receives input from both types of PNs. Since l-ACT neurons may transmit more general and m-ACT neurons more specific information about the quality of the odor (see below), KCs would extract the relevant information most effectively if they were particularly sensitive to the timing of spike arrival within an odor puff. This is exactly what we find.