Aging is associated with cognitive impairment in numerous animal species. Across taxa, decline in learning performance is linked to chronological age. The honey bee (Apis mellifera), in contrast, offers an opportunity to study such aspects of aging largely independent of age per se. This is because foraging onset can be decoupled from chronological age, although workers typically first perform tasks inside the nest and later forage outside the hive. Further, early phases of foraging are characterized by growth of specific brain neuropiles, whereas late phases of the forager life-stage are accompanied by accelerated rates of physiological senescence. Yet, it is unclear if these patterns of senescence include cognitive function. The flexibility of worker ontogeny, however, suggests that the bee can become an attractive model for studies of plasticity in cognitive aging that ultimately may lead to insight into mechanisms that govern age-related cognitive decline. To address this potential, we studied effects of honey bee chronological age and of social role on sensory sensitivity and associative olfactory learning performance. Our results show a decline in olfactory acquisition performance that is linked to social role, but not to chronological age. This decline occurs only in foragers with long foraging duration, but at the same time the foragers show less generalization of odors, which is indicative of more precise learning. Foragers that are reversed from foraging to nest tasks, furthermore, do not show deficits in olfactory acquisition. These results point to complex effects of aging on associative learning in honey bees.

SUMMARYHoney bees (Apis mellifera) are well known for their excellent learning abilities. Although most age groups learn quickly to associate an odor with a sucrose reward, newly emerged bees and old foragers often perform poorly. For a long time, the reason for the poor learning performance of these age groups was unclear. We show that reduced sensitivity for sucrose is the cause for poor associative learning in newly emerged bees but not in old foragers. By increasing the sensitivity for sucrose through octopamine, we selectively improved the learning performance of insensitive newly emerged bees. Interestingly, the learning performance of foragers experiencing the same treatment remained low, despite the observed increase in sensitivity for the reward. We thus demonstrate that increasing sensitivity for the reward can improve the associative learning performance of bees when they are young but not when they had foraged for a long time. Importantly, octopamine can have very different effects on bees, depending on their initial sensory sensitivity. These differential effects of octopamine have important consequences for interpreting the action of biogenic amines on insect behavior.

Ageing is often accompanied by a decline in learning and memory abilities across the animal kingdom. Understanding age-related changes in cognitive abilities is therefore a major goal of current research. The honey bee is emerging as a novel model organism for age-related changes in brain function, because learning and memory can easily be studied in bees under controlled laboratory conditions. In addition, genetically similar workers naturally display life expectancies from 6 weeks (summer bees) to 6 months (winter bees). We studied whether in honey bees, extreme longevity leads to a decline in cognitive functions. Six-month-old winter bees were conditioned either to odours or to tactile stimuli. Afterwards, long-term memory and discrimination abilities were analysed. Winter bees were kept under different conditions (flight/no flight opportunity) to test for effects of foraging activity on learning performance. Despite their extreme age, winter bees did not display an age-related decline in learning or discrimination abilities, but had a slightly impaired olfactory long-term memory. The opportunity to forage indoors led to a slight decrease in learning performance. This suggests that in honey bees, unlike in most other animals, age per se does not impair associative learning. Future research will show which mechanisms protect winter bees from age-related deficits in learning.

The honey bee is a model organism for studies on the neural substrates of learning and memory. Associative olfactory learning using sucrose rewards is fast and reliable in foragers and older hive bees. However, researchers have so far failed to show any significant learning in newly emerged bees. It is generally argued that in these bees only part of the brain structures important for learning are fully developed. Here we show for the first time that newly emerged honey bees are capable of associative learning, if they are sufficiently responsive to sucrose. Responsiveness to sucrose, which can be measured using the proboscis extension response (PER), increases with age. Newly emerged bees are on average very unresponsive to sucrose. We show that if newly emerged bees displaying a PER to 10% sucrose or lower sucrose concentrations are conditioned to an odour, they show significant associative learning and early long-term memory. Nevertheless, the level of acquisition is still lower than in foragers. The general assumption that newly emerged honey bees are incapable of associative learning must therefore be reconsidered. Further, our study suggests that an age-dependent increase in responsiveness to rewarding stimuli is directly related to the development of early learning abilities. The decisive influence of responsiveness to rewarding stimuli in associative learning of newly emerged bees has far reaching consequences for studies on the development of associative learning capabilities in insects and vertebrates.