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First published online August 30, 2006
Journal of Experimental Biology 209, 3587-3598 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02423

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Odour-evoked responses to queen pheromone components and to plant odours using optical imaging in the antennal lobe of the honey bee drone Apis mellifera L.

Jean-Christophe Sandoz

Research Centre for Animal Cognition, UMR 5169, Université Paul Sabatier, 118, Route de Narbonne, 31062 Toulouse cedex 4, France

View larger version (58K): [in a new window]   Fig. 1. Calcium signals in the drone antennal lobe. (A) Anatomical layout of the regions of the drone antennal lobe accessible to optical imaging experiments. An anatomical staining (Neutral Red) of the two antennal lobes of a drone, indicating a ventral region rich in ordinary glomeruli, and a dorsal region containing 2 macroglomeruli (MG1 and MG2). AN, antennal nerve; v, ventral; d, dorsal. Scale bar, 100 µm. (B) Calcium signals in a drone. Upper left: antennal lobe layout of the drone for which the calcium signals are presented. l, lateral; m, medial. Right: activity maps for odour-induced calcium signals in a drone antennal lobe. Relative fluorescence changes (F/F%), taken between the maximum after 1 s and the minimum after 9 s (see C) are presented in a false-colour code, from dark blue to red for different floral odorants (linalool, 1-hexanol, methylsalicylate), a floral blend (orange oil), social pheromones (geraniol and citral) and queen pheromonal components (9-ODA, HVA). Different odours induce different activity patterns, either in the region of ordinary glomeruli or in MG2. (C) Typical time course of relative fluorescence changes (F/F%) in the course of a recording. The presented signal was recorded in MG2 in response to the queen pheromonal component 9-ODA.

View larger version (79K): [in a new window]   Fig. 2. Inter-individual conservation and bilateral symmetry of odour-induced signals in the drone antennal lobe. (A) Calcium signals obtained in five different drones (1-5), on three left and two right antennal lobes (AL) to the odours 1-hexanol and 9-ODA. Each activity map (calculated as in Fig. 1) is scaled to its own minimum and maximum. While 1-hexanol triggers in all five antennal lobes, a similar pattern of a few activated glomeruli [in particular a large egg-shaped glomerulus (H) on the ventro-lateral side], 9-ODA induces activity almost exclusively in the large dorso-lateral region corresponding to MG2. The arrangement of activated glomeruli is symmetrical in left and right antennal lobes. (B) Simultaneous bilateral optical imaging of the drone AL. On the left, a view of the brain showing the recording window and the localisation of the ALs. Scale bar, 100 µm. On the right, a recording to 1-hexanol showing symmetrical activity patterns in four glomeruli in each lobe. Note that glomerulus H can be identified in both lobes. OL, optic lobe; MB, mushroom bodies; v, ventral; d, dorsal.

View larger version (37K): [in a new window]   Fig. 3. Response spectra recorded in identified glomeruli of the drone antennal lobe. (A) Amplitude of calcium responses (F/F%, positive signal 1 s after odour onset) to queen pheromone components and control stimuli recorded in the two macroglomeruli (boxed; mean ± s.e.m., N=11 drones). Only the major component 9-ODA induces clear calcium signals in MG2. MG1 does not respond. ***P<0.001 for all pair-wise Scheffé comparisons. (B) Comparison of responses in three different regions (F1-3; boxed) of MG2 in a subset of the drones (N=5), to the queen pheromone components, the control stimuli and all floral odours in common for these drones. No difference is observed between the response spectra of the three foci: all respond specifically to 9-ODA. (HEX, 1-hexanol; LIO, linalool; ORA, orange oil). (C) Responses of two ordinary glomeruli (boxed) responding to the pheromone components HOB (ventral glomerulus) and HVA (central glomerulus), respectively, in the five drones in which these glomeruli were clearly seen. Responses to the queen pheromone components, the control stimuli and all floral odours in common for these drones are presented (NON, 1-nonanol; LIM, limonene; CLV, clove oil).

View larger version (30K): [in a new window]   Fig. 4. Combinatorial activity patterns to floral odours in the drone antennal lobe and comparison of similarity relationships between drones and workers. (A) Combinatorial response table in a drone. Responses to queen pheromone components, control stimuli and floral odours in ten ordinary glomeruli (Glo.1-10) are colour-coded according to the relative amplitude of the response in this individual. Floral odours induce activity in a combination of ordinary glomeruli. (B) Schematic anatomical layout of the antennal lobe for the same drone as in A. The glomeruli that could be recognised in different individuals (N=5) from their response spectrum, relative position, size and shape are presented in different colours, with their main activating odours. (C) Cluster analyses showing similarity relationships between odours in drones and in workers (using the Euclidian distance between odours in a putative n-dimensional space corresponding to the n measured glomeruli in each individual). Top: drones (N=5). Bottom: workers [datasets of (Galizia et al., 1999; Sachse et al., 1999)]. Similarity relationships among odours are clearly different in the two datasets. For abbreviations, see legend to Fig. 3.