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      Neural correlates of side-specific odour memory in mushroom body output neurons

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      Proceedings of the Royal Society B: Biological Sciences
      The Royal Society

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          Abstract

          <p class="first" id="d2275026e184">Humans and other mammals as well as honeybees learn a unilateral association between an olfactory stimulus presented to one side and a reward. In all of them, the learned association can be behaviourally retrieved via contralateral stimulation, suggesting inter-hemispheric communication. However, the underlying neuronal circuits are largely unknown and neural correlates of across-brain-side plasticity have yet not been demonstrated. We report neural plasticity that reflects lateral integration after side-specific odour reward conditioning. Mushroom body output neurons that did not respond initially to contralateral olfactory stimulation developed a unique and stable representation of the rewarded compound stimulus (side and odour) predicting its value during memory retention. The encoding of the reward-associated compound stimulus is delayed by about 40 ms compared with unrewarded neural activity, indicating an increased computation time for the read-out after lateral integration. </p>

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          Most cited references40

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          Mushroom body memoir: from maps to models.

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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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              The honeybee as a model for understanding the basis of cognition.

              Honeybees contradict the notion that insect behaviour tends to be relatively inflexible and stereotypical. Indeed, they live in colonies and exhibit complex social, navigational and communication behaviours, as well as a relatively rich cognitive repertoire. Because these relatively complex behaviours are controlled by a brain consisting of only 1 million or so neurons, honeybees offer an opportunity to study the relationship between behaviour and cognition in neural networks that are limited in size and complexity. Most recently, the honeybee has been used to model learning and memory formation, highlighting its utility for neuroscience research, in particular for understanding the basis of cognition.
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                Author and article information

                Journal
                Proceedings of the Royal Society B: Biological Sciences
                Proc. R. Soc. B
                The Royal Society
                0962-8452
                1471-2954
                December 14 2016
                December 14 2016
                December 14 2016
                December 14 2016
                : 283
                : 1844
                : 20161270
                Article
                10.1098/rspb.2016.1270
                5204139
                27974514
                dae4465c-6c2b-4440-a64f-bb338ee22dde
                © 2016

                http://royalsocietypublishing.org/licence

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