Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster.

Wustmann, G.; Heisenberg, Martin

doi:10.1101/lm.4.4.328

Cited by 43 publications

(36 citation statements)

References 14 publications

(13 reference statements)

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“…An instrument more suitable than the fs for using the powerful genetic techniques in Drosophila for operant conditioning is the heat box (Wustmann et al, 1996;Wustmann and Heisenberg, 1997;Putz and Heisenberg, 2002). In the tiny, dark chamber, every time the fly walks into a designated half, the whole chamber is heated.…”

Section: Invertebrate Composite Operant Conditioningmentioning

confidence: 99%

Cognition in Invertebrates

Menzel

Brembs

Giurfa

2007

Evolution of Nervous Systems

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Section: Invertebrate Composite Operant Conditioningmentioning

confidence: 99%

Cognition in Invertebrates

Menzel

Brembs

Giurfa

2007

Evolution of Nervous Systems

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“…To investigate this link in flies, we assessed learning and memory in Hk Ϫ mutants by using a heat-box paradigm (Wustmann et al, 1996;Wustmann and Heisenberg, 1997;Putz and Heisenberg, 2002). In this paradigm, single flies were tested in a rectangular chamber divided in half such that the temperature on either side can be controlled independently.…”

Section: Mutations In Hk and Sh Reduce Performance In A Learning And mentioning

confidence: 99%

Drosophila HyperkineticMutants Have Reduced Sleep and Impaired Memory

Bushey¹,

Huber²,

Tononi³

et al. 2007

J. Neurosci.

151

133

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In mammals, sleep is thought to be important for health, cognition, and memory. Fruit flies share most features of mammalian sleep, and a recent study found that Drosophila lines carrying loss-of-function mutations in Shaker (Sh) are short sleeping, suggesting that the Sh current plays a major role in regulating daily sleep amount. The Sh current is potentiated by a ␤ modulatory subunit coded by Hyperkinetic (Hk). Here, we demonstrate that severe loss-of-function mutations of Hk reduce sleep and do so primarily by affecting the Sh current. Moreover, we prove, using a transgenic approach, that a wild-type copy of Hk is sufficient to restore normal sleep. Furthermore, we show that short-sleeping Hk mutant lines have a memory deficit, whereas flies carrying a weaker hypomorphic Hk allele have normal sleep and normal memory. By comparing six short-sleeping Sh lines with two normal sleeping ones, we also found that only alleles that reduce sleep also impair memory. These data identify a gene, Hk, which is necessary to maintain normal sleep, and provide genetic evidence that short sleep and poor memory are linked.Key words: Drosophila; sleep; learning; memory; Shaker; hyperkinetic IntroductionSleep is thought to be important for health, cognition, and memory (Horne, 1988;Bonnet and Arand, 1997;Durmer and Dinges, 2005). Many features of sleep are shared between mammals and fruit flies. As in mammals, sleep in Drosophila consists of long periods of behavioral immobility with increased arousal threshold (Hendricks et al., 2000;Shaw et al., 2000), is associated with changes in brain electrical activity (Nitz and Tononi, 2002) and gene expression (Cirelli et al., 2005a;Zimmerman et al., 2006), is reduced by caffeine and stimulants (Shaw et al., 2000;Hendricks et al., 2003a;Andretic et al., 2005), and becomes fragmented with aging (Koh et al., 2006). In both mammals and flies, sleep is homeostatically regulated, because its duration and intensity increase with the duration of previous waking (Huber et al., 2004), and sleep deprivation (SD) results in reduced performance (Huber et al., 2004).In a recent study, we found that Sh mns flies, which carry a point mutation in a conserved Shaker (Sh) domain, sleep only 3-4 h/d, whereas their wild-type controls sleep 8 -14 h/d (Cirelli et al., 2005b). After crossing out genetic modifiers accumulated over many generations, we found that other Sh alleles become short sleepers and fail to complement the short sleeping Sh mns phenotype, suggesting that the Sh current is responsible for the short sleeping phenotype. The Sh locus encodes the ␣ subunit of a tetrameric potassium channel that passes a voltage-activated fastinactivating (I A ) current (Schwarz et al., 1988). Sh orthologs (K v ) occur in vertebrates (Littleton and Ganetzky, 2000) and, in both mammals and flies, play a major role in the control of membrane repolarization and transmitter release (Schwarz et al., 1988). Hyperkinetic (Hk) encodes a ␤ subunit that binds to each ␣ subunit in the Sh tetramer ( Fig. 1), and its presenc...

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“…A memory posttest (the chamber is now permanently cool) shows the persistence in avoidance of the chamber half associated with an elevated temperature. The change in time spent in one chamber half over the other is used as a quantitative measure of memory formation (Wustmann and Heisenberg 1997;Putz and Heisenberg 2002). On average, wild-type flies typically have little to no spontaneous preference, as indicated in the pre-test phase in the sample experiment (B).…”

Section: Reinforcer/memory Level Relationshipmentioning

confidence: 99%

“…In the honeybee and Drosophila, octopamine is important for positive, and dopamine (so far only shown in Drosophila) for negative associations (Hammer and Menzel 1998;Menzel et al 1999;Schwaerzel et al 2003). Despite the well-accepted notion that the biogenic amines are involved in reinforcement, little is known of the circuits that feed into or out of this system or how the teaching neurons regulate the graded release of neurotransmitter.A fast operant learning paradigm, the heat-box, lends itself to a genetic dissection of the reinforcement intensity/memory strength relationship in Drosophila (Wustmann and Heisenberg 1997;Putz and Heisenberg 2002). In this paradigm, single flies are allowed to run freely in a dark chamber that is lined top and bottom with heating elements (Fig.…”

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confidence: 99%

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Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila

Diegelmann¹,

Zars²,

Zars³

2006

Learn. Mem.

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Memories can have different strengths, largely dependent on the intensity of reinforcers encountered. The relationship between reinforcement and memory strength is evident in asymptotic memory curves, with the level of the asymptote related to the intensity of the reinforcer. Although this is likely a fundamental property of memory formation, relatively little is known of how memory strength is determined. Memory performance at different levels in Drosophila can be measured in an operant heat-box conditioning paradigm. In this spatial learning paradigm, flies learn and remember to avoid one-half of a dark chamber associated with a temperature outside of the preferred range. The reinforcement temperature has a strong effect on the level of learning in wild-type flies, with higher temperatures inducing stronger memories. Additionally, two mutations alter memory-acquisition curves, either changing acquisition rate or asymptotic memory level. The rutabaga mutation, affecting a type-1 adenylyl cyclase, decreases the acquisition rate. In contrast, the white mutation, modifying an ABC transporter, limits asymptotic memory. The white mutation does not negatively affect classical olfactory conditioning but actually improves performance at low reinforcement levels. Thus, memory acquisition/memory strength and classical olfactory/operant spatial memories can be genetically dissociated. A conceptual model of operant conditioning and the levels at which rutabaga and white influence conditioning is proposed.Memories are formed from unexpected experiences. Eventually, a sensory cue or behavior predicts positive or negative consequences. Importantly, memory strength depends on the intensity of those reinforcing stimuli such that weak reinforcers support memories of limited magnitude. This relationship is evident in asymptotic acquisition curves where the asymptote level is related to the intensity of the reinforcer. This has been found in operant and classical conditioning paradigms with both positive and negative reinforcers in many species (Herrnstein 1997), including several species of insects (e.g., in rewarded classical and operant conditioning in the honeybee and negatively associated olfactory classical conditioning in Drosophila) (Menzel and Erber 1972;Bitterman et al. 1983;Tully and Quinn 1985;Loo and Bitterman 1992). The repeated finding of the positive relationship between reinforcement intensity and memory strength indicates that this is a fundamental property of learning.The biogenic amines (e.g., serotonin, dopamine, and octopamine) can function as teaching signals. These are the molecules that, together with sensory-based depolarization, feed into the cAMP/PKA and NMDA-receptor pathways. The biochemical changes in this pathway support synaptic plasticity and memory formation. In the Aplysia model of heterosynaptic plasticity, serotonin mediates the tail shock and is a sufficient teaching signal with in vitro synaptic plasticity tests (Martin et al. 1997;Kandel 2001). Dopamine is also critical in memory formation....

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Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster.

Cited by 43 publications

References 14 publications

Cognition in Invertebrates

Cognition in Invertebrates

Drosophila HyperkineticMutants Have Reduced Sleep and Impaired Memory

Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila

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