The carrot, not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae

Hendel, Thomas; Michels, Birgit; Neuser, Kirsa; Schipanski, Angela; Kaun, Karla R.; Sokolowski, Marla B.; Marohn, Frank; Michel, René; Heisenberg, Martin; Gerber, Bertram

doi:10.1007/s00359-004-0574-8

Cited by 65 publications

(73 citation statements)

References 35 publications

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“…Injections of octopamine into bees depleted of biogenic amines by reserpine can restore the reinforcing function of sucrose during conditioning, but octopamine does not rescue the response-releasing function as measured in sensitization experiments (Menzel et al 1999). In Drosophila larvae, it was shown that stimuli that strongly affect response-releasing behavior, such as the attractant fructose or the repellent quinine, do not necessarily affect olfactory choice behaviors and thus seem ineffective as reinforcers (Hendel et al 2005).…”

Section: Discussion Us Evaluation and Acquisitionmentioning

confidence: 99%

Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees

Scheiner¹,

Kuritz-Kaiser²,

Menzel³

et al. 2005

Learn. Mem.

101

127

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In tactile learning, sucrose is the unconditioned stimulus and reward, which is usually applied to the antenna to elicit proboscis extension and which the bee can drink when it is subsequently applied to the extended proboscis. The conditioned stimulus is a tactile object that the bee can scan with its antennae. In this paper we describe the quantitative relationships between gustatory antennal stimulation, gustatory proboscis stimulation, and tactile learning and memory. Bees are 10-fold more responsive to sucrose solutions when they are applied to the antenna compared to proboscis stimulation. During tactile conditioning, the sucrose solution applied to the proboscis determines the level of acquisition, whereas antennal input is of minor importance. Bees differing in their gustatory responsiveness measured at the antenna differ strongly in their tactile acquisition and memory. We demonstrate how these differences in tactile acquisition and memory can be greatly reduced by calculating equal subjective rewards, based on individual gustatory responsiveness.Learning in animals depends on many factors including the salience of the conditioned stimulus (CS) and the strength of the unconditioned stimulus (US) (Rescorla and Wagner 1972). Even under controlled laboratory conditions, individuals show variance in the rate of acquisition, the asymptote of acquisition, and in retention (Scheiner et al. 2001a(Scheiner et al. ,b, 2003Matzel et al. 2003;Hedden and Gabrieli 2004;Dellu-Hagedorn 2005). Multiple intrinsic factors can contribute to these behavioral differences. Some of these factors may be related to individual differences in evaluating CS and US (Scheiner et al. 1999;Chester et al. 2003). These differences could reflect genetic heterogeneity at the individual level.Studies in honeybees (Apis mellifera L.) can be very useful to identify important factors leading to inter-individual learning differences and their potential sources of control. Associative learning plays an important part in honeybee behavior. Bees learn very fast the location of a foraging site and the numerous characteristics of reward-yielding plants (for review, see Menzel

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Section: Discussion Us Evaluation and Acquisitionmentioning

confidence: 99%

Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees

Scheiner¹,

Kuritz-Kaiser²,

Menzel³

et al. 2005

Learn. Mem.

101

127

View full text Add to dashboard Cite

show abstract

“…Associative learning was indicated by systematic differences in test performance between the reciprocal treatment conditions. The reciprocally trained groups were run alternately, which allows stringent pairing of data for the calculation of a performing index (PI) [see below and discussion in Hendel et al (2005)]. For a differential, two-odor version of our paradigm (Fig.…”

Section: Methodsmentioning

confidence: 99%

Behavioral and Synaptic Plasticity Are Impaired upon Lack of the Synaptic Protein SAP47

Saumweber¹,

Weyhersmüller²,

Hallermann³

et al. 2011

J. Neurosci.

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The synapse-associated protein of 47 kDa (SAP47) is a member of a phylogenetically conserved gene family of hitherto unknown function. In Drosophila, SAP47 is encoded by a single gene (Sap47) and is expressed throughout all synaptic regions of the wild-type larval brain; specifically, electron microscopy reveals anti-SAP47 immunogold labeling within 30 nm of presynaptic vesicles. To analyze SAP47 function, we used the viable and fertile deletion mutant Sap47 156 , which suffers from a 1.7 kb deletion in the regulatory region and the first exon. SAP47 cannot be detected by either immunoblotting or immunohistochemistry in Sap47 156 mutants. These mutants exhibit normal sensory detection of odorants and tastants as well as normal motor performance and basic neurotransmission at the neuromuscular junction. However, short-term plasticity at this synapse is distorted. Interestingly, Sap47 156 mutant larvae also show a 50% reduction in odorant-tastant associative learning ability; a similar associative impairment is observed in a second deletion allele (Sap47 201 ) and upon reduction of SAP47 levels using RNA interference. In turn, transgenically restoring SAP47 in Sap47 156 mutant larvae rescues the defect in associative function. This report thus is the first to suggest a function for SAP47. It specifically argues that SAP47 is required for proper behavioral and synaptic plasticity in flies-and prompts the question whether its homologs are required for proper behavioral and synaptic plasticity in other species as well.

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“…You therefore need to compare experimentally naïve animals of the different genotypes in terms of (1) their preference between fructose and plain agarose (see Hendel et al 2005;Niewalda et al 2008;or Schipanski et al 2008 for how to do this), (2) their preference between an AM-filled and an empty container, as well as (3) their preference between an OCT-filled and an empty container.…”

Section: Experimental Designmentioning

confidence: 99%

Odor–Taste Learning Assays in Drosophila Larvae

Gerber¹,

Biernacki²,

Thum³

2013

Cold Spring Harb Protoc

Self Cite

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The Drosophila larva is an emerging model for studies in behavioral neurogenetics because of its simplicity in terms of cell number. Despite this simplicity, basic features of neuronal organization and key behavior faculties are shared with adult flies and with mammals. Here, we describe a Pavlovian-type learning assay in fruit fly larvae. A group of larvae is sequentially exposed to specific odors in the presence or the absence of sugar, and then tested to determine whether they prefer the odor previously experienced with the reward. The protocol uses a two-group, reciprocal training design: One group of Drosophila larvae is exposed to n-amyl acetate (AM) with a sugar reward (+), then subsequently exposed to 1-octanol (OCT) with no reward (denoted AM+/OCT). The other group receives the reciprocal training (AM/OCT+). The two groups of larvae are then tested for their choices between AM and OCT. Relatively higher preferences for AM after AM+/OCT training than after AM/ OCT+ training reflect associative learning and are quantified by the learning index (LI). This method offers a robust, simple, cheap, and reasonably quick test for learning ability (an aversive version is available as well, using either high-concentration salt or quinine as punishment). With the concerted efforts of the Drosophila research community, we anticipate it will allow us to unravel the full circuitry underlying odor-taste learning on a single-cell level. MATERIALSIt is essential that you consult the appropriate Material Safety Data Sheets and your institution's Environmental Health and Safety Office for proper handling of equipment and hazardous materials used in this protocol. ReagentsAgarose, 1% solution in distilled water Agarose, 1% solution, supplemented with 2 M fructose or sucrose Drosophila larvaeFlies are reared in culture bottles at 25˚C, with a relative atmospheric humidity of 60%-70% and with a 14/10-h light/dark cycle. Five-day-old larvae are used (90-120 h after egg laying); in particular, only larvae that are still in the food paste, and not larvae that may have begun to crawl up the side of the glass (known as the "wandering stage"), should be used for the learning assay.

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The carrot, not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae

Cited by 65 publications

References 35 publications

Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees

Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees

Behavioral and Synaptic Plasticity Are Impaired upon Lack of the Synaptic Protein SAP47

Odor–Taste Learning Assays in Drosophila Larvae

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