Structured sampling of olfactory input by the fly mushroom body

Abstract

15Associative memory formation and recall in the adult fruit fly Drosophila melanogaster is 16 subserved by the mushroom body (MB). Upon arrival in the MB, sensory information undergoes 17 a profound transformation. Olfactory projection neurons (PNs), the main MB input, exhibit 18 broadly tuned, sustained, and stereotyped responses to odorants; in contrast, their postsynaptic 19 targets in the MB, the Kenyon cells (KCs), are nonstereotyped, narrowly tuned, and only briefly 20 responsive to odorants. Theory and experiment have suggested that this transformation is 21 implemented by random connectivity between KCs and PNs. However, this hypothesis has been 22 challenging to test, given the difficulty of mapping synaptic connections between large numbers 23 of neurons to achieve a unified view of neuronal network structure. Here we used a recent 24 whole-brain electron microscopy (EM) volume of the adult fruit fly to map large numbers of PN-25 to-KC connections at synaptic resolution. Comparison of the observed connectome to precisely 26 defined null models revealed unexpected network structure, in which a subset of food-responsive 27 PN types converge on individual downstream KCs more frequently than expected. The 28 connectivity bias is consistent with the neurogeometry: axons of the overconvergent PNs tend to 29 arborize near one another in the MB main calyx, making local KC dendrites more likely to 30 receive input from those types. Computational modeling of the observed PN-to-KC network 31showed that input from the overconvergent PN types is better discriminated than input from 32 other types. These results suggest an 'associative fovea' for olfaction, in that the MB is wired to 33 better discriminate more frequently occurring and ethologically relevant combinations of food-34 related odors. 35 36 45 (DasGupta et al., 2014; Dickinson and Muijres, 2016; Ofstad et al., 2011; Owald and Waddell, 46 2015); and the stereotyped morphology and physiology of its cell types allow ready integration 47 of information across individuals (Costa et al., 2016; Nern et al., 2015). Each cell type normally 48

The connectome of the adultDrosophilamushroom body: implications for function

“…First, although olfactory input to the KCs is highly mixed, various structural features reduce the dimensionality of the KC odor representation. A recent analysis of EM data from an adult Drosophila MB identified groups of PNs thought to represent food odors that are preferentially sampled by certain KCs (Zheng et al, 2020). Consistent with this observation, our analysis revealed subtype-specific biases in PN sampling by KCs, including an overrepresentation of specific glomeruli by α/β and α′/β′ KCs.…”

“…This maintained segregation is most prominent for α′/β′ KCs but is also seen in α/β KCs ( Figure 5E-G). The dendrites of each KC type also tend to be found in the same region of the CA (Video 6; Leiss et al, 2009;Lin et al, 2007;Zheng et al, 2020), which, in some cases, appears to support input specialization. These features of the spatial mapping from CA to lobes and the organisation of the parallel fiber system presumably evolved to facilitate associative learning.…”

“…This requirement, together with global feedback inhibition (Lin et al, 2014a;Papadopoulou et al, 2011), ensures a sparse representation where only a small percentage of KCs are activated by an odor (Honegger et al, 2011;Perez-Orive et al, 2002). The MB has a three layered divergent-convergent architecture (Huerta et al, 2004;Jortner et al, 2007;Laurent, 2002;Litwin-Kumar et al, 2017;Shomrat et al, 2011;Stevens, 2015) in which the coherent information represented by olfactory PNs is expanded and decorrelated when delivered to the KCs (Caron et al, 2013;Zheng et al, 2020). But the degree to which the structure of the sensory input representation is maintained by the KCs has been debated.…”

Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain

“…Some food-related odor channels may directly facilitate the action of others. A new study observed a community of PNs in the MB CA, a food-related “associational fovea”, densely sampled by a population of KCs [ 68 ]. This community is almost identical to the food-related, axo-axonic community we observe in the LH (note that both studies use the same EM data).…”

Information flow, cell types and stereotypy in a full olfactory connectome

“…In addition, we compare and validate results using a second EM data set, the full adult fly brain (FAFB, (Zheng et al, 2018)), which has been used until now for sparse manual circuit tracing (e.g. (Dolan et al, 2018; Dolan et al, 2019; Sayin et al, 2019; Felsenberg et al, 2018; Huoviala et al, 2018; Zheng et al, 2020; Marin et al, 2020; Bates et al, 2020; Otto et al, 2020; Coates et al, 2020)).…”