Differential odor processing in two olfactory pathways in the honeybee

Yamagata, Nobuhiro; Schmuker, Michael; Szyszka, Paul; Mizunami, Makoto; Menzel, Randolf

doi:10.3389/neuro.06.016.2009

Cited by 62 publications

(107 citation statements)

References 62 publications

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“…While the quality of an odour may be coded for memory formation by the unique set of Kenyon cells it activates, its intensity may be coded for example by the level of activity summed across all antennal lobe glomeruli, as previously argued with respect to adult Drosophila as well as the honey bee (Borst, 1983;Sachse and Galizia, 2003;Yamagata et al, 2009;Schmuker et al, 2011). Both larval and adult antennal lobes harbour inhibitory interneurons innervating various numbers of glomeruli; also, excitatory interneurons with similarly wide connectivity are found in the adult antennal lobe [larva (Python and Stocker, 2002a;Python and Stocker, 2002b;Asahina et al, 2009;Thum et al, 2011); adult (Wilson and Laurent, 2005;Olsen et al, 2007;Shang et al, 2007;Chou et al, 2010;Huang et al, 2010;Seki et al, 2010;Yaksi and Wilson, 2010); for a particularly detailed anatomical analysis, see Tanaka et al (Tanaka et al, 2012)].…”

Section: Possible Circuitry Underlying Intensity Learningmentioning

confidence: 99%

Olfactory memories are intensity specific in larval Drosophila

Mishra

Chen

Yarali

et al. 2013

Journal of Experimental Biology

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SUMMARYLearning can rely on stimulus quality, stimulus intensity, or a combination of these. Regarding olfaction, the coding of odour quality is often proposed to be combinatorial along the olfactory pathway, and working hypotheses are available concerning short-term associative memory trace formation of odour quality. However, it is less clear how odour intensity is coded, and whether olfactory memory traces include information about the intensity of the learnt odour. Using odour-sugar associative conditioning in larval Drosophila, we first describe the dose-effect curves of learnability across odour intensities for four different odours (n-amyl acetate, 3-octanol, 1-octen-3-ol and benzaldehyde). We then chose odour intensities such that larvae were trained at an intermediate odour intensity, but were tested for retention with either that trained intermediate odour intensity, or with respectively higher or lower intensities. We observed a specificity of retention for the trained intensity for all four odours used. This adds to the appreciation of the richness in ʻcontentʼ of olfactory short-term memory traces, even in a system as simple as larval Drosophila, and to define the demands on computational models of associative olfactory memory trace formation. We suggest two kinds of circuit architecture that have the potential to accommodate intensity learning, and discuss how they may be implemented in the insect brain. Supplementary material available online at

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Section: Possible Circuitry Underlying Intensity Learningmentioning

confidence: 99%

Olfactory memories are intensity specific in larval Drosophila

Mishra

Chen

Yarali

et al. 2013

Journal of Experimental Biology

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“…In many cases, myogram recordings of the muscle M17 (Rehder 1987), a muscle which controls the proboscis extension, were used to monitor the bees' responses under experimental conditions that do not allow free movements of the proboscis. Although some parts of the CS pathway are still only superficially characterized (for instance, the lateral horn), and we are only beginning to understand temporal aspects of odorant processing at several stages of this pathway (Szyszka et al 2005;Fernandez et al 2009;Yamagata et al 2009;Denker et al 2010), an integrative view of the CS circuit is already available.…”

Section: Neural Bases Of Cs and Us Processingmentioning

confidence: 99%

“…Thus, calcium signals in the bee brain could, to some extent, allow prediction of the bees' generalization behavior with odorants. This research now needs to be extended to other brain regions downstream from the antennal lobe, such as the mushroom bodies, where neural activity maps can be recorded (Faber and Menzel 2001;Szyszka et al 2005;Yamagata et al 2009) and their predictive power with respect to behavioral PER measures can be assessed. PER conditioning has Figure 5.…”

Section: Per Conditioning and The Study Of Olfactory Perceptionmentioning

confidence: 99%

“…Neural activity at the different stages of this CS processing pathway has been measured using a variety of recording techniques including electrophysiological and optophysiological methods (Mauelshagen 1993;Joerges et al 1997;Abel et al 2001;Szyszka et al 2005;Yamagata et al 2009;Denker et al 2010). In many cases, myogram recordings of the muscle M17 (Rehder 1987), a muscle which controls the proboscis extension, were used to monitor the bees' responses under experimental conditions that do not allow free movements of the proboscis.…”

Section: Neural Bases Of Cs and Us Processingmentioning

confidence: 99%

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Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Giurfa

Sandoz²

2012

Learn. Mem.

346

334

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The honeybee Apis mellifera has emerged as a robust and influential model for the study of classical conditioning, thanks to the existence of a powerful Pavlovian conditioning protocol, the olfactory conditioning of the proboscis extension response (PER). In 2011, the olfactory PER conditioning protocol celebrates 50 years since it was first introduced by Kimihisa Takeda in 1961. Here, we review its origins, developments, and perspectives in order to define future research avenues and necessary methodological and conceptual evolutions. We show that olfactory PER conditioning has become a versatile tool for the study of questions in extremely diverse fields in addition to the study of learning and memory and that it has allowed behavioral characterizations, not only of honeybees, but also of other insect species, for which the protocol was adapted. We celebrate, therefore, Takeda's original work and prompt colleagues to conceive and establish further robust behavioral tools for an accurate characterization of insect learning and memory at multiple levels of analysis.Classical conditioning (Pavlov 1927) is a form of conditioning in which a subject learns to associate a neutral stimulus (the "conditioned stimulus," or CS), which does not originally elicit a behavioral response, with a stimulus of biological significance (the "unconditioned stimulus," or US), which elicits an innate, often reflexive, response. Through this association, the originally neutral stimulus acquires the capacity to elicit a conditioned response.Decades of research on animal learning and memory have established some invertebrates (e.g., the sea hare, Aplysia californica, the fruit fly, Drosophila melanogaster, the honeybee, Apis mellifera) as standard models for the study of classical conditioning (Giurfa 2007b;Menzel et al. 2007). This success can be attributed to the fact that these animals can learn nonassociative as well as Pavlovian and operant associations and possess relatively simple nervous systems that allow retracing of these phenomena to the cellular and molecular levels in different kinds of laboratory preparations. Among these invertebrates, the honeybee, Apis mellifera, has emerged as a robust and influential model for the study of

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“…Olfactory input reaches the MBs via olfactory PNs, which ascend from the antennal lobe. PNs have been characterized in detail in the honeybee (Abel et al, 2001;Szyszka et al, 2005;Krofczik et al, 2008;Yamagata, 2009). In the lip region of the MB calyces, the PNs synapse onto specified KCs (Mobbs, 1982).…”

Section: Introductionmentioning

confidence: 99%

Long-term memory and response generalization in mushroom body extrinsic neurons in the honeybee Apis mellifera

Haehnel

Menzel

2012

Journal of Experimental Biology

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SUMMARYHoneybees learn to associate an odor with sucrose reward under conditions that allow the monitoring of neural activity by imaging Ca 2+ transients in morphologically identified neurons. Here we report such recordings from mushroom body extrinsic neurons -which belong to a recurrent tract connecting the output of the mushroom body with its input, potentially providing inhibitory feedback -and other extrinsic neurons. The neuronsʼ responses to the learned odor and two novel control odors were measured 24h after learning. We found that calcium responses to the learned odor and an odor that was strongly generalized with it were enhanced compared with responses to a weakly generalized control. Thus, the physiological responses measured in these extrinsic neurons accurately reflect what is observed in behavior. We conclude that the recorded recurrent neurons feed information back to the mushroom body about the features of learned odor stimuli. Other extrinsic neurons may signal information about learned odors to different brain regions.

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Differential odor processing in two olfactory pathways in the honeybee

Cited by 62 publications

References 62 publications

Olfactory memories are intensity specific in larval Drosophila

Olfactory memories are intensity specific in larval Drosophila

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Long-term memory and response generalization in mushroom body extrinsic neurons in the honeybee Apis mellifera

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