Abstract
SummaryNervous systems contain sensory neurons, local neurons, projection neurons, and motor neurons. To understand how these building blocks form whole circuits, we must distil these broad classes into neuronal cell types and describe their network connectivity. Using an electron micrograph dataset for an entire Drosophila melanogaster brain, we reconstruct the first complete inventory of olfactory projections connecting the antennal lobe, the insect analog of the mammalian olfactory bulb, to higher-order brain regions in an adult animal brain. We then connect this inventory to extant data in the literature, providing synaptic-resolution “holotypes” both for heavily investigated and previously unknown cell types. Projection neurons are approximately twice as numerous as reported by light level studies; cell types are stereotyped, but not identical, in cell and synapse numbers between brain hemispheres. The lateral horn, the insect analog of the mammalian cortical amygdala, is the main target for this olfactory information and has been shown to guide innate behavior. Here, we find new connectivity motifs, including axo-axonic connectivity between projection neurons, feedback, and lateral inhibition of these axons by a large population of neurons, and the convergence of different inputs, including non-olfactory inputs and memory-related feedback onto third-order olfactory neurons. These features are less prominent in the mushroom body calyx, the insect analog of the mammalian piriform cortex and a center for associative memory. Our work provides a complete neuroanatomical platform for future studies of the adult Drosophila olfactory system.
Highlights
We have a good mechanistic understanding of the principles of information processing in the primary olfactory center where first- and second-order neurons meet; this logic appears very similar between insects and mammals [1, 2]
Using the recent full adult fly brain (FAFB) Electron microscopy (EM) dataset [21], we created a full inventory of antennal lobe (AL) projection neurons (PNs)
In FAFB, we found 347 PNs with dendrites in the right AL
Summary
We have a good mechanistic understanding of the principles of information processing in the primary olfactory center where first- and second-order neurons meet; this logic appears very similar between insects and mammals [1, 2]. The axons of first-order olfactory receptor neurons (ORNs) ramify in 51 distinct olfactory glomeruli, a figure we finalize in the present work. The AL implements local computations, including divisive normalization via lateral inhibition, before projection neurons (PNs; analogous to vertebrate mitral and tufted cells) carry information to higher brain regions (Figure 1A) [2]. Olfactory PNs target multiple brain regions including the well-studied mushroom body (MB), which appears analogous to the mammalian piriform cortex as both areas subserve associative olfactory memory [10,11,12,13] (Figure 1A). This work creates a neuroinformatic scaffold that can integrate diverse data from other studies
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