Functional and anatomical specificity in a higher olfactory centre.

Shahar Frechter,Davi Bock,James Manton,Gregory Jefferis,Arian Rokkum Jamasb,Johannes Kohl,Sina Tootoonian,Michael-John Dolan,Alexander Shakeel Bates

doi:10.7554/elife.44590

Abstract

Most sensory systems are organized into parallel neuronal pathways that process distinct aspects of incoming stimuli. In the insect olfactory system, second order projection neurons target both the mushroom body, required for learning, and the lateral horn (LH), proposed to mediate innate olfactory behavior. Mushroom body neurons form a sparse olfactory population code, which is not stereotyped across animals. In contrast, odor coding in the LH remains poorly understood. We combine genetic driver lines, anatomical and functional criteria to show that the Drosophila LH has ~1400 neurons and >165 cell types. Genetically labeled LHNs have stereotyped odor responses across animals and on average respond to three times more odors than single projection neurons. LHNs are better odor categorizers than projection neurons, likely due to stereotyped pooling of related inputs. Our results reveal some of the principles by which a higher processing area can extract innate behavioral significance from sensory stimuli.

Highlights

In thinking about the transition from stimulus through perception to behavior, chemosensory systems have become increasingly studied due to their relatively shallow architecture: just two synapses separate the sensory periphery from neurons that are believed to form memories or instruct behavior (Wilson and Mainen, 2006; Masse et al, 2009)
Since we found that LH neurons (LHNs) show stereotyped odor responses across animals, we carried out a detailed analysis of neuronal cell types
We identified a total of 261 LHN cell types divided into 34 local cell types (LHLNs) with arbors restricted to the lateral horn (LH) and 227 LH output neurons (LHONs) cell types with axons beyond the LH

Summary

Introduction

In thinking about the transition from stimulus through perception to behavior, chemosensory systems have become increasingly studied due to their relatively shallow architecture: just two synapses separate the sensory periphery from neurons that are believed to form memories or instruct behavior (Wilson and Mainen, 2006; Masse et al, 2009). Are there distinct cell types with reproducible odor responses across animals? What is the nature of the population code in a higher olfactory area linked to innate behavior? Second order neurons make divergent projections onto multiple higher olfactory centers. For example in both flies and mice there are separate projections to areas proposed to be specialized for memory formation

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Conclusion