Reward quality influences the development of learned olfactory biases in honeybees

Wright, Geraldine A.; Choudhary, Amir F.; Bentley, Mark

doi:10.1098/rspb.2009.0040

Cited by 58 publications

(67 citation statements)

References 58 publications

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“…It is unlikely that the asymmetry was due to a preference for 3:7, because a preference for that ratio was not evident with conditioning of 9:1 vs 9:1. A more extensive analysis of peak shift in olfactory conditioning of honey bees can be found in Wright et al (2009b).…”

Section: Resultsmentioning

confidence: 99%

Associative Conditioning Tunes Transient Dynamics of Early Olfactory Processing

Fernández¹,

Locatelli²,

et al. 2009

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Odors evoke complex spatiotemporal responses in the insect antennal lobe (AL) and mammalian olfactory bulb. However, the behavioral relevance of spatiotemporal coding remains unclear. In the present work we combined behavioral analyses with calcium imaging of odor induced activity in the honeybee AL to evaluate the relevance of this temporal dimension in the olfactory code. We used a new way for evaluation of odor similarity of binary mixtures in behavioral studies, which involved testing whether a match of odor-sampling time is necessary between training and testing conditions for odor recognition during associative learning. Using graded changes in the similarity of the mixture ratios, we found high correlations between the behavioral generalization across those mixtures and a gradient of activation in AL output. Furthermore, short odor stimuli of 500 ms or less affected how well odors were matched with a memory template, and this time corresponded to a shift from a sampling-time-dependent to a sampling-time-independent memory. Accordingly, 375 ms corresponded to the time required for spatiotemporal AL activity patterns to reach maximal separation according to imaging studies. Finally, we compared spatiotemporal representations of binary mixtures in trained and untrained animals. AL activity was modified by conditioning to improve separation of odor representations. These data suggest that one role of reinforcement is to "tune" the AL such that relevant odors become more discriminable.

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Section: Resultsmentioning

confidence: 99%

Associative Conditioning Tunes Transient Dynamics of Early Olfactory Processing

Fernández¹,

Locatelli²,

et al. 2009

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“…As the mode of action of neonicotinoids, which are agonists of nAChRs, is different from organophosphates, which are inhibitors of acetylcholinesterase neurotransmitters, the underlying molecular mechanisms of the observed decreases in learning are likely to be somewhat different. Overall, given the importance of olfactory learning in flower recognition and foraging in bees [48], the impaired learning of honeybees exposed to field-realistic levels of clothianidin may have important ecological implications at the colony level, and offers a potential mechanism underlying observed reductions in the homing ability and impaired foraging behaviour of neonicotinoid stressed honeybees [49,50].…”

Section: Discussionmentioning

confidence: 99%

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Piiroinen¹,

Goulson²

2016

Proc. R. Soc. B.

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Learning and memory are crucial functions which enable insect pollinators to efficiently locate and extract floral rewards. Exposure to pesticides or infection by parasites may cause subtle but ecologically important changes in cognitive functions of pollinators. The potential interactive effects of these stressors on learning and memory have not yet been explored. Furthermore, sensitivity to stressors may differ between species, but few studies have compared responses in different species. Here, we show that chronic exposure to fieldrealistic levels of the neonicotinoid clothianidin impaired olfactory learning acquisition in honeybees, leading to potential impacts on colony fitness, but not in bumblebees. Infection by the microsporidian parasite Nosema ceranae slightly impaired learning in honeybees, but no interactive effects were observed. Nosema did not infect bumblebees (3% infection success). Nevertheless, Nosema-treated bumblebees had a slightly lower rate of learning than controls, but faster learning in combination with neonicotinoid exposure. This highlights the potential for complex interactive effects of stressors on learning. Our results underline that one cannot readily extrapolate findings from one bee species to others. This has important implications for regulatory risk assessments which generally use honeybees as a model for all bees.

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“…The bees were retained in the feeding boxes for 3days prior to experimentation. On the 4th day, the entire cohort in each box was cold anaesthetized and each bee was transferred to a restraining harness as described previously (Wright et al, 2009). Each bee was allowed to recover for 1h, fed 25μl of the solution it had experienced for the previous 3days, and left in a humidified plastic box at room temperature overnight.…”

Section: Exposure To Pesticidesmentioning

confidence: 99%

Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees

Williamson

Wright

2013

Journal of Experimental Biology

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266

242

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SUMMARYPesticides are important agricultural tools often used in combination to avoid resistance in target pest species, but there is growing concern that their widespread use contributes to the decline of pollinator populations. Pollinators perform sophisticated behaviours while foraging that require them to learn and remember floral traits associated with food, but we know relatively little about the way that combined exposure to multiple pesticides affects neural function and behaviour. The experiments reported here show that prolonged exposure to field-realistic concentrations of the neonicotinoid imidacloprid and the organophosphate acetylcholinesterase inhibitor coumaphos and their combination impairs olfactory learning and memory formation in the honeybee. Using a method for classical conditioning of proboscis extension, honeybees were trained in either a massed or spaced conditioning protocol to examine how these pesticides affected performance during learning and short-and long-term memory tasks. We found that bees exposed to imidacloprid, coumaphos, or a combination of these compounds, were less likely to express conditioned proboscis extension towards an odor associated with reward. Bees exposed to imidacloprid were less likely to form a long-term memory, whereas bees exposed to coumaphos were only less likely to respond during the short-term memory test after massed conditioning. Imidacloprid, coumaphos and a combination of the two compounds impaired the beesʼ ability to differentiate the conditioned odour from a novel odour during the memory test. Our results demonstrate that exposure to sublethal doses of combined cholinergic pesticides significantly impairs important behaviours involved in foraging, implying that pollinator population decline could be the result of a failure of neural function of bees exposed to pesticides in agricultural landscapes. Supplementary material available online at

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Reward quality influences the development of learned olfactory biases in honeybees

Cited by 58 publications

References 58 publications

Associative Conditioning Tunes Transient Dynamics of Early Olfactory Processing

Associative Conditioning Tunes Transient Dynamics of Early Olfactory Processing

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees

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