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First published online November 2, 2007
Journal of Experimental Biology 210, 4024-4033 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.006585

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Olfactory memory formation and the influence of reward pathway during appetitive learning by honey bees

Geraldine A. Wright^1,*,, Julie A. Mustard^2,*, Sonya M. Kottcamp³ and Brian H. Smith²

¹ Division of Biology, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK
² School of Life Sciences, Arizona State University, PO Box 874501, Tempe, AZ 85287, USA
³ Rothenbuhler Honeybee Laboratory, Ohio State University, Columbus, OH 43210, USA

View larger version (15K): [in this window] [in a new window]   Fig. 1. Rates of acquisition for honey bees trained with three different conditioning protocols reflected in the mean (± s.e.m.) response on each trial. (A) APC protocol where both antennae and proboscis are stimulated with sucrose solution and the bees are allowed to consume the sucrose reward (Npollen=65; Nnectar=63). (B) PC protocol where only the proboscis is stimulated and bees are then allowed to consume the reward (Npollen=78; Nnectar=69). (C) AC protocol where the antennae are stimulated with sucrose solution, but subjects were not allowed to touch the sucrose solution with their proboscis or consume the reward (Npollen=60; Nnectar=65). The rate of acquisition was greatest for the APC protocol; honey bees conditioned using the PC or AC protocols did not have significantly different rates of acquisition. The predicted probability of responding on each conditioning trial is shown with the ± s.e.m. of this probability. Abbreviations: Pol, pollen foragers; Nect, nectar foragers; +, reinforced trials with CS odor on the A trials; –, B trials with the unreinforced odor.

View larger version (12K): [in this window] [in a new window]   Fig. 2. Recall is greatest immediately after conditioning, and the rate of memory decay depends on the protocol used for conditioning. The proportion of honey bees responding to the rewarded odor during the first recall test trial at different times after conditioning is shown. (A) Pollen foragers were conditioned using the APC, PC or AC regime and then tested for recall immediately (NAPC=22; NAC=22; NPC=21), after 24 h (NAPC=25; NAC=29; NPC=24) or 96 h (NAPC=20; NAC=21; NPC=19). (B) Nectar foragers were conditioned using one of the three training protocols and were then tested for recall immediately (NAPC=17; NAC=23; NPC=23) or 24 h later (NAPC=21; NAC=26; NPC=22) or 96 h later (NAPC=22; NAC=22; NPC=21). Recall for AC and PC was compared to that for APC using a least-squares contrast at each time point; * indicates a difference of P<0.05.

View larger version (4K): [in this window] [in a new window]   Fig. 3. An odor paired with stimulation of the antennae produces associative learning. Pollen foragers conditioned with forward pairing of the odor and sucrose stimulation of only the antennae demonstrated the most robust conditioning. Recall of honey bees receiving backward or unpaired conditioning of odor with antennal-only stimulation was significantly lower than that of the forward-paired subjects ( 22=7.45, P=0.024). The proportion of bees responding to the conditioned odor during two recall tests is shown (Nforward=22; Nbackward=21; Nunpaired=23).

View larger version (6K): [in this window] [in a new window]   Fig. 4. Conditioning protocol also affects recall after single-trial conditioning. The proportion of subjects responding to the first recall test with the rewarded odor immediately (NAPC=35; NAC=40; NPC=33; NUNP=31), 24 h (NAPC=39; NAC=25; NPC=42; NUNP=29) or 96 h (NAPC=48; NAC=75; NPC=30; NUNP=22) after conditioning is shown. None of the honey bees trained with the unpaired protocol responded on the immediate recall test. Recall at each time post-conditioning depended upon the conditioning protocol (lreg; 23=39.6, P<0.001). Recall of the odor CS decays for all conditioning protocols (APC, PC, AC) over a period of 96 h (lreg; 22=6.27, P=0.043). Recall for AC, PC and UNP was compared to that for APC using a least-squares contrast at each time point; * indicates a difference of P<0.05.

View larger version (11K): [in this window] [in a new window]   Fig. 5. The presence of sucrose in the reward strongly affects the ability of honey bees to recall the olfactory CS. Pollen foragers were conditioned with the APC protocol, the antennal-stimulation-alone (AC) protocol or a protocol where the antennae were stimulated with sucrose solution but the subject was fed water (ACW). (A) The rate of acquisition was greatest for the APC protocol (lreg; 22=7.80, P=0.040) (NAPC=69; NAC=58; NACW=68). (B) When tested immediately after conditioning, the level of response of subjects to the CS during the first recall trial was not significantly different for the three protocols ( 22=1.60, P=0.449) (NAPC=35; NAC=29; NACW=31). After 24 h, the response of the AC and ACW subjects was significantly lower than the responses of the APC subjects ( 22=9.21, P=0.010) (NAPC=34; NAC=29; NACW=37). *P<0.05.