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      From Antenna to Antenna: Lateral Shift of Olfactory Memory Recall by Honeybees

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          Honeybees, Apis mellifera, readily learn to associate odours with sugar rewards and we show here that recall of the olfactory memory, as demonstrated by the bee extending its proboscis when presented with the trained odour, involves first the right and then the left antenna. At 1–2 hour after training using both antennae, recall is possible mainly when the bee uses its right antenna but by 6 hours after training a lateral shift has occurred and the memory can now be recalled mainly when the left antenna is in use. Long-term memory one day after training is also accessed mainly via the left antenna. This time-dependent shift from right to left antenna is also seen as side biases in responding to odour presented to the bee's left or right side. Hence, not only are the cellular events of memory formation similar in bees and vertebrate species but also the lateralized networks involved may be similar. These findings therefore seem to call for remarkable parallel evolution and suggest that the proper functioning of memory formation in a bilateral animal, either vertebrate or invertebrate, requires lateralization of processing.

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          Most cited references23

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          Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization.

          Recent evidence in natural and semi-natural settings has revealed a variety of left-right perceptual asymmetries among vertebrates. These include preferential use of the left or right visual hemifield during activities such as searching for food, agonistic responses, or escape from predators in animals as different as fish, amphibians, reptiles, birds, and mammals. There are obvious disadvantages in showing such directional asymmetries because relevant stimuli may be located to the animal's left or right at random; there is no a priori association between the meaning of a stimulus (e.g., its being a predator or a food item) and its being located to the animal's left or right. Moreover, other organisms (e.g., predators) could exploit the predictability of behavior that arises from population-level lateral biases. It might be argued that lateralization of function enhances cognitive capacity and efficiency of the brain, thus counteracting the ecological disadvantages of lateral biases in behavior. However, such an increase in brain efficiency could be obtained by each individual being lateralized without any need to align the direction of the asymmetry in the majority of the individuals of the population. Here we argue that the alignment of the direction of behavioral asymmetries at the population level arises as an "evolutionarily stable strategy" under "social" pressures occurring when individually asymmetrical organisms must coordinate their behavior with the behavior of other asymmetrical organisms of the same or different species.
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            Classical conditioning of proboscis extension in honeybees (Apis mellifera).

            Extension of the proboscis was conditioned in restrained honeybees with odor as the conditioned stimulus (CS) and sucrose solution--delivered to the antenna (to elicit extension of the proboscis) and then to the proboscis itself--as the unconditioned stimulus (US). In a first series of experiments, acquisition was found to be very rapid, both in massed and in spaced trials; its associative basis was established by differential conditioning and by an explicitly unpaired control procedure (which produced marked resistance to acquisition in subsequent paired training); and both extinction and spontaneous recovery in massed trials were demonstrated. In a series of experiments on the nature of the US, eliminating the proboscis component was found to lower the asymptotic level of performance, whereas eliminating the antennal component was without effect; reducing the concentration of sucrose from 20% to 7% slowed acquisition but did not lower the asymptotic level of performance; and second-order conditioning was demonstrated. In a series of experiments on the role of the US, an omission contingency designed to eliminate adventitious response-reinforcer contiguity was found to have no adverse effect on acquisition. In a series of experiments designed to analyze the resistance to acquisition found after explicitly unpaired training in the first experiments, no significant effect was found of prior exposure either to the CS alone or to the US alone, although the unpaired procedure again produced substantial resistance that was shown to be due to inhibition rather than to inattention; extinction after paired training was found to be facilitated by unpaired presentations of the US. The relation between these results for honeybees and those of analogous experiments with vertebrates is considered.
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              Searching for the memory trace in a mini-brain, the honeybee.

              R. Menzel (2001)
              To determine general or species-specific properties in neural systems, it is necessary to use comparative data in evaluating experimental findings. Presented here are data on associative learning and memory formation in honeybees, emphasizing a comparative approach. We focus on four aspects: (1) the role of an identified neuron, VUM(mx1), as a neural substrate of appetitive reinforcement; (2) the sequences of molecular events as they correlate with five forms of memory stages; (3) the localization of the memory traces following appetitive olfactory learning; and (4) the brief description of several forms of complex learning in bees (configuration in olfactory conditioning, categorization in visual feature learning, delayed matching-to-sample learning, and latent learning in navigation). VUM(mx1) activity following the conditioned stimulus odor is sufficient to replace the unconditioned stimulus, and VUM(mx1) changes its response properties during learning similarly to what is known from dopamine neurons in the basal ganglia of the mammalian brain. The transition from short- to mid- and long-term forms of memory can be related to specific activation of second messenger cascades (involving NOS, PKA, PKC, and PKM) resembling general features of neural plasticity at the cellular level. The particular time course of the various memory traces may be adapted to the behavioral context in which they are used; here, the foraging cycle of the bee. Memory traces for even such a simple form of learning as olfactory conditioning are multiple and distributed, involving first- and second-order sensory neuropils (antennal lobe and mushroom bodies), but with distinctly different properties. The wealth of complex forms of learning in the context of foraging indicates basic cognitive capacities based on rule extraction and context-dependent learning. It is believed that bees might be a useful model for studying cognitive faculties at a middle level of complexity.

                Author and article information

                Role: Editor
                PLoS ONE
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                4 June 2008
                : 3
                : 6
                : e2340
                [1 ]Centre for Neuroscience and Animal Behaviour, University of New England, Armidale, Australia
                [2 ]Centre for Mind/Brain Sciences, University of Trento, Rovereto, Italy
                University of Cambridge, United Kingdom
                Author notes

                Conceived and designed the experiments: GV LR. Performed the experiments: GV LR. Analyzed the data: GV LR. Wrote the paper: GV LR.

                Rogers, Vallortigara. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                : 4 April 2008
                : 28 April 2008
                Page count
                Pages: 5
                Research Article
                Neuroscience/Animal Cognition



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