A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body

By Jena L. Pitman, Wolf Huetteroth, Christopher J. Burke, M. Krashes, Sen-Lin Lai, Tzumin Lee, S. Waddell. 2011

134 citations recorded by the source corpus.

Summary Labile memory is thought to be held in the brain as persistent neural network activity [1–4]. However, it is not known how biologically relevant memory circuits are organized and operate. Labile and persistent appetitive memory in Drosophila requires output after training from the α′β′ subset of mushroom body (MB) neurons and from a pair of modulatory Dorsal Paired Medial (DPM) neurons [5–9]. DPM neurons innervate the entire MB lobe region and appear to be pre- and post-synaptic to the MB [7, 8], consistent with a recurrent network model. Here we identify a role after training for synaptic output from the GABAergic Anterior Paired Lateral (APL) neurons [10, 11]. Blocking synaptic output from APL neurons after training disrupts labile memory but does not affect long-term memory. APL neurons contact DPM neurons most densely in the α′β′ lobes although their processes are intertwined and contact throughout all the lobes. Furthermore, APL contacts MB neurons in the α′ lobe but makes little direct contact with those in the distal α lobe. We propose that APL neurons provide widespread inhibition to stabilize and maintain synaptic specificity of a labile memory trace in a recurrent DPM and MB α′β′ neuron circuit.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics

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Citations in the corpus

Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, neutral): “, 2005) (gift from Andre Fiala, University of Göttingen); MB247-LexA (Pitman et al., 2011) (gift from Scott Waddell, University of Oxford); LexAOP-P2X2 (Yao et al.”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “Two memory processes that are thought to rely on different molecular and circuit mechanisms, anesthesia resistant memory and anesthesia sensitive memory, contribute to memory at this retention time (Dudai et al., 1976; Folkers et al., 1993; Isabel et al., 2004; Krashes and Waddell, 2008; Aso et al.,”
Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila (2015, methodology): “GRASP experiments were performed as described (Gordon and Scott, 2009; Pitman et al., 2011).”
Origins of Cell-Type-Specific Olfactory Processing in the Drosophila Mushroom Body Circuit. (2017, unknown): “This is in line with the anatomical observation that APL neurons contact most densely with a0/b0 KCs in the lobes (Pitman et al., 2011).”
Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit (2015, background): “FB inhibition exists in the MB of fly, cockroach, locust, honeybee, and mammal [13, 14, 16, 17].”
A connectome of a learning and memory center in the adult Drosophila brain (2017, background): “…2011) and GABA (Haynes et al., 2015) as neurotransmitters; its role in the circuit is less clear, but it is gap-junctionally coupled to APL (Wu et al., 2011), and appears to be important for memory consolidation (Yu et al., 2005a; Pitman et al., 2011; Figure 6 continued Figure 6—source data 1).”
Sweet Taste and Nutrient Value Subdivide Rewarding Dopaminergic Neurons in Drosophila (2015, background): “41 mM Na2HPO4, and 175 mM NaCl) and fixed for an additional 60 min at room temperature [19].”
Parallel processing of appetitive short- and long-term memories in Drosophila. (2011, background): “And it was recently shown that blocking GABAergic anterior paired lateral (APL) neurons, which project onto the MB lobes and dendrites, for 2 hr after appetitive conditioning affects STM but not LTM [35].”
Dopamine activity in projection neurons regulates short‐lasting olfactory approach memory in Drosophila (2022, background): “GH146-GAL4 drives GAL4 expression in anterior paired lateral (APL) neurons as well as PNs (Liu & Davis, 2009; Pitman et al., 2011; Wu et al., 2013), while a second driver, NP225-GAL4 (Tanaka et al., 2004), expresses strongly in the PNs, but not in APL neurons (Zhou et al., 2019).”
A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster (2015, background): “…al., 2000), c305a-GAL4 (Krashes et al., 2007), NP2721-GAL4 (Wu et al., 2011), VT64246-GAL4 (Lee et al., 2011), MB247GAL4 (Zars, 2000), MB247-lexA (Pitman et al., 2011), R58E02-lexA (Liu et al., 2012), MB-GAL80 (Thum et al., 2007), eyeless-GAL80 (Chotard et al., 2005), ptub-GAL80ts (McGuire et…”
Modelling learning and memory in Drosophila to understand Intellectual Disabilities. (2020, unknown): “Furthermore, GABAergic inputs to the MB, such as the anterior paired lateral neurons and the dorsal paired medial neurons, are implicated in behavioral flexibility, learning and memory consolidation (Lin et al., 2014a; Liu and Davis, 2009; Pitman et al., 2011; Ren et al., 2012; Wu et al., 2012).”
Transposition Driven Genomic Heterogeneity in the Drosophila Brain: A Dissertation (2012, unknown): “We used a previously described MB-expressing LexA transgene, 247-LexA::VP16 (Pitman et al., 2011) to express a lexA-operator driven FLP recombinase (lexAop-FLP) (Shang et al., 2008) in combination with different MB-GAL4 drivers expressing the UAS>STOP>mCD8::GFP transgene (where “>” denotes a FLP…”
Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability (2012, background): “Alternatively, subcellular memory traces may interact at the circuit level via interneurons, such as the DPM and APL neurons, for which previous studies showed their essential role in memory consolidation [6,38,49,50].”
Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila (2013, methodology): “We expressed a membrane-tethered GFP (uasmCD8::GFP) using the c739, 0770, NP7175, and c708a GAL4 drivers and localized expression within the overall MB neurons using a LexAop-rCD2::RFP transgene driven by 247-LexA::VP16 (Pitman et al., 2011).”
Functional analysis of a higher olfactory center, the lateral horn (2012, background): “…lateral neuron (APL), which may contribute to olfactory memory, is the only known GABAergic neuron projecting to the calyx (Liu and Davis, 2009; Pitman et al., 2011; Wu et al., 2011); it is morphologically and physiologically similar to the locust GGN (Papadopoulou et al., 2011), although its…”