The neuronal architecture of the mushroom body provides a logic for associative learning

By Yoshinori Aso, Daisuke Hattori, Yang Yu, R. Johnston, N. Iyer, Teri-Tb Ngo, Heather Dionne, L. F. Abbott, R. Axel, Hiromu Tanimoto and 1 more. 2014

898 citations recorded by the source corpus.

We identified the neurons comprising the Drosophila mushroom body (MB), an associative center in invertebrate brains, and provide a comprehensive map describing their potential connections. Each of the 21 MB output neuron (MBON) types elaborates segregated dendritic arbors along the parallel axons of ∼2000 Kenyon cells, forming 15 compartments that collectively tile the MB lobes. MBON axons project to five discrete neuropils outside of the MB and three MBON types form a feedforward network in the lobes. Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments. Convergence of DAN axons on compartmentalized Kenyon cell–MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations. The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory. DOI: http://dx.doi.org/10.7554/eLife.04577.001

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics, Neuroscience, Cognitive Science & Psychology

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Citations in the corpus

Genetic dissection of mutual interference between two consecutive learning tasks in Drosophila (2022, background): “Pro-I is reduced by overexpressing CSW in MB γ Neurons The MB contains ~2,000 intrinsic neurons called Kenyon cells (KCs), which are further divided into three major types: γ neurons (~675), α/β neurons (~990), and α’/β’neurons (~350) (Aso et al., 2014).”
CoSCL: Cooperation of Small Continual Learners is Stronger than a Big One (2022, neutral): “e, sub-networks) to process sequential experiences in parallel, and integrates their outputs in a weighted-sum fashion to guide adaptive behaviors [3, 9, 30].”
Dopaminergic neurons write and update memories with cell-type-specific rules (2016, neutral): “DOI: 10.7554/eLife.16135.001”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “The MBONs, as the only known efferent pathways of the mushroom body, must translate KC odor representations into adaptive behavioral responses (Aso et al., 2014a; Tanaka et al., 2008).”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, methodology): “As pointed out in (Aso et al., 2014), this circuit structure is well-suited to deal with conflicts between long-lasting memory traces and the need to adapt to survive in a dynamic environment where the meaning of a given sensory input may change.”
Recognition (2003, neutral): “Previous olfactory computation literature has explored robustness and associative learning (Babadi & Sompolinsky, 2014; Aso et al., 2014).”
Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila (2022, background): “To invariantly test whether the observed recovery was attributable to α2 expressed in α’3 MBONs, we trained animals while knocking down α2 specifically in α’3 MBONs (α2GFP and MB027B Split- Gal4 >UAS-α2RNAi).”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, positive): “MB299B-GAL4 has strong expression in PAM-α1 (Aso et al., 2014a; Yamagata et al., 2015) (Figure 3B).”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, positive): “The MB contains both intrinsic neurons (termed Kenyon cells or KCs) and extrinsic neurons (comprising output neurons (MBONs), neurons postsynaptic to the KCs, and several types of modulatory neuron) (Aso et al., 2014a; Tanaka et al., 2008).”
Do the right thing: neural network mechanisms of memory formation, expression and update in Drosophila (2018, background): “The presynaptic terminals of different subsets of dopaminergic neurons (DANs), encoding positive or negative valence, occupy distinct, nonoverlapping compartments of the mushroom body neuropil which are precisely matched by the dendritic fields of discrete MBONs (Figure 1) [16,18,19,22,23,34 ,35,36]”
Fast and sensitive GCaMP calcium indicators for imaging neural populations (2021, neutral): “05) and comparable to 8m (84[32-165] ms) and XCaMP-Gf (91[48-155] ms) (Fig.”
A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila. (2015, methodology): “21 different types of MBONs provide KC output to convergent regions in the dorsal protocerebrum [16, 17].”