Random Convergence of Olfactory Inputs in the Drosophila Mushroom Body

By S. Caron, V. Ruta, L. F. Abbott, Richard Axel. 2013

426 citations recorded by the source corpus.

The mushroom body in the fruitfly Drosophila melanogaster is an associative brain centre that translates odour representations into learned behavioural responses. Kenyon cells, the intrinsic neurons of the mushroom body, integrate input from olfactory glomeruli to encode odours as sparse distributed patterns of neural activity. We have developed anatomic tracing techniques to identify the glomerular origin of the inputs that converge onto 200 individual Kenyon cells. Here we show that each Kenyon cell integrates input from a different and apparently random combination of glomeruli. The glomerular inputs to individual Kenyon cells show no discernible organization with respect to their odour tuning, anatomic features or developmental origins. Moreover, different classes of Kenyon cells do not seem to preferentially integrate inputs from specific combinations of glomeruli. This organization of glomerular connections to the mushroom body could allow the fly to contextualize novel sensory experiences, a feature consistent with the role of this brain centre in mediating learned olfactory associations and behaviours.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics, Computational Biology & Bioinformatics, Neuroscience

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Citations in the corpus

Re-evaluating circuit mechanisms underlying pattern separation (2019, positive): “Projection neurons integrate signals from stereotyped sets of glomeruli, which form random synaptic connections onto Kenyon cells in the mushroom body calyx (Figure 2B) (Masuda-Nakagawa et al., 2005; Murthy et al., 2008; Caron et al., 2013; but see Eichler et al., 2017; Zheng et al., 2018).”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “In the mushroom body, odors are encoded as sparse ensembles of activated Kenyon cells (KCs) (Campbell et al., 2013), each of which integrates input from diverse combinations of olfactory glomeruli in the calyx (Caron et al., 2013; Gruntman and Turner, 2013).”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “…whose parallel axonal fibers form the MB lobes (Crittenden et al., 1998; Aso et al., 2009), are not stereotyped (Figure 1A) (Murthy et al., 2008; Caron et al., 2013); that is, individual flies show distinct wiring patterns between projection neurons and KCs. Sparse activity of the KCs…”
Recognition (2003, positive): “Individual KCs receive unstructured input from ∼ 4 − 10 PNs (Caron et al., 2013; Li et al., 2020; Zheng et al., 2018), and piriform neurons receive roughly 30 − 100 inputs from a random collection of glomeruli (Davison & Ehlers, 2011; Miyamichi et al., 2011).”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, background): “4 inputs from a random combination of glomeruli; that is, knowledge of a single input to a KC provides no information about the identity of the additional inputs, and connections differ in different flies (Murthy et al., 2008; Caron et al., 2013; Gruntman and Turner, 2013).”
Clique topology reveals intrinsic geometric structure in neural correlations (2015, background): “Alternatively, a correlation or connectivity matrix could be truly unstructured, such as the connectivity pattern observed in the fly olfactory system (2), indicating random network organization.”
Origins of Cell-Type-Specific Olfactory Processing in the Drosophila Mushroom Body Circuit. (2017, neutral): “Importantly, each KC receives on average seven inputs from a random set of PNs (Caron et al., 2013) with some local rules (Gruntman and Turner, 2013).”
Neuronal mechanisms underlying innate and learned olfactory processing in Drosophila. (2019, background): “This connectivity is not stereotyped [58,59], but is 178 also not purely stochastic, as PNs with similar odor tuning profiles, and from the same 179 glomeruli, tend to converge on the same KCs [57,60].”
The Olfactory System (2014, background): “The neuronal hardwiring of odorant coding that exists in the olfactory bulb does not seem to exist within the regions of the brain that are involved in olfaction and odor perception (Caron et al. 2013; Sosulski et al. 2011).”
Why neurons mix: high dimensionality for higher cognition. (2016, background): “strategy to expand dimensionality in the olfactory system of the drosophila [52 ].”
Distinct dopamine neurons mediate reward signals for short- and long-term memories (2014, background): “This also implies undefined anatomical connectivity of some PAM neurons and the input neurons, as in the connectivity between the projection neurons and the Kenyon cells (44, 45).”