A Pair of Inhibitory Neurons Are Required to Sustain Labile Memory in the Drosophila Mushroom Body

Pitman, Jena L.; Huetteroth, Wolf; Burke, Christopher; Krashes, Michael J.; Lai, Sen-Lin; Lee, Tzumin; Waddell, Scott

doi:10.1016/j.cub.2011.03.069

Cited by 125 publications

(149 citation statements)

References 42 publications

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“…Blocking the synaptic output from g lobe or a/b lobe neurons impairs the retrieval of aversive 3-h memory Aversive and appetitive 3-h memories formed after one-session training are typical memory phases (intermediate-term memory) for studying different processes of olfactory memory processing, including memory acquisition, consolidation, and retrieval (McGuire et al 2001;Keene et al 2006;Krashes et al 2007;Pitman et al 2011;Berry et al 2012). shibire ts1 is a dominant temperature-sensitive allele of dynamin (Kim and Wu 1990;Kitamoto 2001;Kasuya et al 2009).…”

Section: Resultsmentioning

confidence: 99%

Requirement of the combination of mushroom body γ lobe and α/β lobes for the retrieval of both aversive and appetitive early memories in Drosophila

Xie

Huang

et al. 2013

Learn. Mem.

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Extensive studies of Drosophila mushroom body in formation and retrieval of olfactory memories allow us to delineate the functional logic for memory storage and retrieval. Currently, there is a questionable disassociation of circuits for memory storage and retrieval during Drosophila olfactory memory processing. Formation of the initial aversive olfactory memory involves mushroom body γ lobe, whereas α/β lobes are reported to be necessary for the retrieval of such memory. In contrast, formation and retrieval of the short-term appetitive olfactory memory appears to involve γ lobe. With the help of newly identified Gal4 lines and of focusing on 3-h memory for both aversive and appetitive conditionings, our reexamination of the retrieval of aversive and appetitive olfactory memories suggests a new view. Blocking γ lobe output led to severe deficiency of aversive early memory retrieval and partial impairment of appetitive early memory retrieval. Interrupting α/β lobe output impaired the retrieval of both aversive and appetitive early memories. The contribution of the γ lobe and α/β lobes appeared to be additive for the retrieval of appetitive early memory. Thus, these results suggest that the retrieval of aversive and appetitive olfactory early memories requires the synaptic outputs from both γ lobe and α/β lobe neurons. This discovery may help us to rethink how aversive and appetitive memories are processed from memory formation to memory retrieval.

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Section: Resultsmentioning

confidence: 99%

Requirement of the combination of mushroom body γ lobe and α/β lobes for the retrieval of both aversive and appetitive early memories in Drosophila

Xie

Huang

et al. 2013

Learn. Mem.

View full text Add to dashboard Cite

show abstract

“…Here, aversive and appetitive memories can be compared in a site-bysite manner (Schwaerzel et al, 2003). The quality of the behavioral reinforcer used during the training procedure, i.e., either sugar reward for appetitive learning or electric shock punishment for aversive learning, influences the neuronal circuits (Krashes et al, 2007(Krashes et al, , 2009Pitman et al, 2011) required to establish an appropriate memory at the level of the Drosophila MBs (Schwaerzel et al, 2003;Thum et al, 2007). When assayed for immediate aversive or appetitive memory performance, rg 1 and rg ␥5 animals show a significant reduction compared with wild-type Canton-S controls.…”

Section: Resultsmentioning

confidence: 99%

Drosophila rugoseIs a Functional Homolog of MammalianNeurobeachinand Affects Synaptic Architecture, Brain Morphology, and Associative Learning

Volders

Scholz²,

Slabbaert

et al. 2012

J. Neurosci.

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Neurobeachin (Nbea) is implicated in vesicle trafficking in the regulatory secretory pathway, but details on its molecular function are currently unknown. We have used Drosophila melanogaster mutants for rugose (rg), the Drosophila homolog of Nbea, to further elucidate the function of this multidomain protein. Rg is expressed in a granular pattern reminiscent of the Golgi network in neuronal cell bodies and colocalizes with transgenic Nbea, suggesting a function in secretory regulation. In contrast to Nbea Ϫ/Ϫ mice, rg null mutants are viable and fertile and exhibit aberrant associative odor learning, changes in gross brain morphology, and synaptic architecture as determined at the larval neuromuscular junction. At the same time, basal synaptic transmission is essentially unaffected, suggesting that structural and functional aspects are separable. Rg phenotypes can be rescued by a Drosophila rg؉ transgene, whereas a mouse Nbea transgene rescues aversive odor learning and synaptic architecture; it fails to rescue brain morphology and appetitive odor learning. This dissociation between the functional redundancy of either the mouse or the fly transgene suggests that their complex composition of numerous functional and highly conserved domains support independent functions. We propose that the detailed compendium of phenotypes exhibited by the Drosophila rg null mutant provided here will serve as a test bed for dissecting the different functional domains of BEACH (for beige and human Chediak-Higashi syndrome) proteins, such as Rugose, mouse Nbea, or Nbea orthologs in other species, such as human.

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“…Clonal analysis of the GH146-Gal4 revealed that the projection of the APL neuron formed a continuous net-like innervation throughout the compartment of the ipsilateral MB except the cell body region (Liu and Davis, 2009). They inhibit olfactory learning (Liu and Davis, 2009), but promote stabilization of labile olfactory memory traces (Pitman et al, 2011;Wu et al, 2011).…”

Section: The Apl Neurons Are Required For Visual Reversal Learningmentioning

confidence: 99%

A GABAergic Inhibitory Neural Circuit Regulates Visual Reversal Learning inDrosophila

Ren

et al. 2012

J. Neurosci.

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Inflexible cognition and behavior are prominent features of prefrontal cortex damage and several neuropsychiatric disorders. The ability to flexibly adapt cognitive processing and behavior to dynamically changing environmental contingencies has been studied using the reversal learning paradigm in mammals, but the complexity of the brain circuits precludes a detailed analysis of the underlying neural mechanism. Here we study the neural circuitry mechanism supporting flexible behavior in a genetically tractable model organism, Drosophila melanogaster. Combining quantitative behavior analysis and genetic manipulation, we found that inhibition from a single pair of giant GABAergic neurons, the anterior paired lateral (APL) neurons, onto the mushroom bodies (MBs) selectively facilitates behavioral flexibility during visual reversal learning. This effect was mediated by ionotropic GABA A receptors in the MB. Moreover, flies with perturbed MB output recapitulated the poor reversal performance of flies with dysfunctional APL neurons. Importantly, we observed that flies with dysfunctional APL-MB circuit performed normally in simple forms of visual learning, including initial learning, extinction, and differential conditioning. Finally, we showed that acute disruption of the APL-MB circuit is sufficient to impair visual reversal learning. Together, these data suggest that the APL-MB circuit plays an essential role in the resolution of conflicting reinforcement contingencies and reveals an inhibitory neural mechanism underlying flexible behavior in Drosophila.

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A Pair of Inhibitory Neurons Are Required to Sustain Labile Memory in the Drosophila Mushroom Body

Cited by 125 publications

References 42 publications

Requirement of the combination of mushroom body γ lobe and α/β lobes for the retrieval of both aversive and appetitive early memories in Drosophila

Requirement of the combination of mushroom body γ lobe and α/β lobes for the retrieval of both aversive and appetitive early memories in Drosophila

Drosophila rugoseIs a Functional Homolog of MammalianNeurobeachinand Affects Synaptic Architecture, Brain Morphology, and Associative Learning

A GABAergic Inhibitory Neural Circuit Regulates Visual Reversal Learning inDrosophila

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