Plasticity-driven individualization of olfactory coding in mushroom body output neurons

By Toshihide Hige, Yoshinori Aso, Gerald M. Rubin, Glenn C. Turner. 2015

149 citations recorded by the source corpus.

Although all sensory circuits ascend to higher brain areas where stimuli are represented in sparse, stimulus-specific activity patterns, relatively little is known about sensory coding on the descending side of neural circuits, as a network converges. In insects, mushroom bodies have been an important model system for studying sparse coding in the olfactory system, where this format is important for accurate memory formation. In Drosophila, it has recently been shown that the 2,000 Kenyon cells of the mushroom body converge onto a population of only 34 mushroom body output neurons (MBONs), which fall into 21 anatomically distinct cell types. Here we provide the first, to our knowledge, comprehensive view of olfactory representations at the fourth layer of the circuit, where we find a clear transition in the principles of sensory coding. We show that MBON tuning curves are highly correlated with one another. This is in sharp contrast to the process of progressive decorrelation of tuning in the earlier layers of the circuit. Instead, at the population level, odour representations are reformatted so that positive and negative correlations arise between representations of different odours. At the single-cell level, we show that uniquely identifiable MBONs display profoundly different tuning across different animals, but that tuning of the same neuron across the two hemispheres of an individual fly was nearly identical. Thus, individualized coordination of tuning arises at this level of the olfactory circuit. Furthermore, we find that this individualization is an active process that requires a learning-related gene, rutabaga. Ultimately, neural circuits have to flexibly map highly stimulus-specific information in sparse layers onto a limited number of different motor outputs. The reformatting of sensory representations we observe here may mark the beginning of this sensory-motor transition in the olfactory system.

Subfields: Cellular and Molecular Neuroscience, Genetics, Sensory Systems

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Citations in the corpus

Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “MBON axons converge on a small number of target neuropils, where their concerted activity has been proposed to bias an animal's innate and learned olfactory preferences (Aso et al., 2014b; Hige et al., 2015; Owald et al., 2015).”
A connectome of a learning and memory center in the adult Drosophila brain (2017, background): “Previous electrophysiological measurements of connectivity in the a2 compartment indicated that only about 30% of KCs connect to MBON-a2sc (Hige et al., 2015b), suggesting the possibility that the majority of KC>MBON synapses are functionally silent, as they are in cerebellar cortex, where 98% of th”
Modelling learning and memory in Drosophila to understand Intellectual Disabilities. (2020, unknown): “This process is believed to form the neural basis of olfactory associative learning (Heisenberg, 2003; Schwaerzel et al., 2003; Kim et al., 2007; Burke et al., 2012; Liu et al., 2012; Qin et al., 2012; Cohn et al., 2015; Hige et al., 2015; Owald and Waddell, 2015; Rohwedder et al., 2016; Kaun and Ro”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, unknown): “…2014a) and that functional roles of specific cell types are being worked out in detail (Aso et al., 2014b; Chen et al., 2012; Cohn et al., 2015; Hige et al., 2015a; Hige et al., 2015b; Owald et al., 2015; Sejourne et al., 2011), our study provides a timely addition to the mushroom body…”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, unknown): “Furthermore, odor-tuning patterns of some MBONs are diverse across naive animals, suggesting that MBON responses are individualized through experience-dependent plasticity (Hige et al., 2015).”
A Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster (2017, background): “…al., 2017; Ofstad et al., 2011; Owald and Waddell, 2015; Pavlou and Goodwin, 2013; von Reyn et al., 2014), electrophysiological accessibility (e.g. Hige et al., 2015; Wilson et al., 2004), relatively small size (Figure 1A), and the stereotypy of and genetic access to most of the ~100,000 neurons…”