Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila
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Evaluation Summary:
Information about the environment obtained through sensory organs is processed and utilized at multiple levels in the brain. In this study, the authors use a variety of modern genetic and optophysiological tools to uncover the function and connectivity of glutamatergic neurons in a higher brain center of Drosophila - the lateral horn. They find that these neurons do not only encode chemical odor identity, but also the hedonic value (attractive or repulsive) of odors. This advances our understanding of how odors are represented in the brain will be of value to those who are interested in odour coding and behavioural valence of various odours.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)
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Abstract
Understanding neuronal representations of odor-evoked activities and their progressive transformation from the sensory level to higher brain centers features one of the major aims in olfactory neuroscience. Here, we investigated how odor information is transformed and represented in higher-order neurons of the lateral horn, one of the higher olfactory centers implicated in determining innate behavior, using Drosophila melanogaster . We focused on a subset of third-order glutamatergic lateral horn neurons (LHNs) and characterized their odor coding properties in relation to their presynaptic partner neurons, the projection neurons (PNs) by two-photon functional imaging. We show that odors evoke reproducible, stereotypic, and odor-specific response patterns in LHNs. Notably, odor-evoked responses in these neurons are valence-specific in a way that their response amplitude is positively correlated with innate odor preferences. We postulate that this valence-specific activity is the result of integrating inputs from multiple olfactory channels through second-order neurons. GRASP and micro-lesioning experiments provide evidence that glutamatergic LHNs obtain their major excitatory input from uniglomerular PNs, while they receive an odor-specific inhibition through inhibitory multiglomerular PNs. In summary, our study indicates that odor representations in glutamatergic LHNs encode hedonic valence and odor identity and primarily retain the odor coding properties of second-order neurons.
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Evaluation Summary:
Information about the environment obtained through sensory organs is processed and utilized at multiple levels in the brain. In this study, the authors use a variety of modern genetic and optophysiological tools to uncover the function and connectivity of glutamatergic neurons in a higher brain center of Drosophila - the lateral horn. They find that these neurons do not only encode chemical odor identity, but also the hedonic value (attractive or repulsive) of odors. This advances our understanding of how odors are represented in the brain will be of value to those who are interested in odour coding and behavioural valence of various odours.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the …
Evaluation Summary:
Information about the environment obtained through sensory organs is processed and utilized at multiple levels in the brain. In this study, the authors use a variety of modern genetic and optophysiological tools to uncover the function and connectivity of glutamatergic neurons in a higher brain center of Drosophila - the lateral horn. They find that these neurons do not only encode chemical odor identity, but also the hedonic value (attractive or repulsive) of odors. This advances our understanding of how odors are represented in the brain will be of value to those who are interested in odour coding and behavioural valence of various odours.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
In this manuscript, the authors investigate odour representation in the lateral horn (LH). They first map neurons of various neurotranmistter identities using photoactivation of GFP in the LH then focus the rest of their analysis on glutamatergic LHNs. They show that LHNs and uniglomerular PNs show 1) stereotypic representations of odours in the LH, 2) that attractive odours (represented more strongly) and aversive odours (represented more weakly) are spatially segregated in the LH. They perform correlations of response profiles to suggest that the response pf the LHN, which itself correlates with behavioural valence, is not acquired from the OSN or PN.
Finally, they address connectivity using GRASP and laser microdissections. Using GRASP, they show that glutamatergic LHNs are presynaptic to both uni- and …
Reviewer #1 (Public Review):
In this manuscript, the authors investigate odour representation in the lateral horn (LH). They first map neurons of various neurotranmistter identities using photoactivation of GFP in the LH then focus the rest of their analysis on glutamatergic LHNs. They show that LHNs and uniglomerular PNs show 1) stereotypic representations of odours in the LH, 2) that attractive odours (represented more strongly) and aversive odours (represented more weakly) are spatially segregated in the LH. They perform correlations of response profiles to suggest that the response pf the LHN, which itself correlates with behavioural valence, is not acquired from the OSN or PN.
Finally, they address connectivity using GRASP and laser microdissections. Using GRASP, they show that glutamatergic LHNs are presynaptic to both uni- and multi-glomerualar PNs. Using laser ablations they propose that that LHNs receive excitatory input from the uniglomerular PNs and inhibitory input from the multiglomerular PNs and that the inhibition shapes the LHN responses to odours.
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Reviewer #2 (Public Review):
The fruit fly represents an excellent model organism to analyze in detail how odor stimuli are processed by brain circuits at different levels of complexity. Whereas much insight has been gained in recent years about peripheral processes at the level of sensory neurons and the primary circuits within the antennal lobes, the roles and interplay of the many and diverse neurons at higher brain levels such as the lateral horn remain less clear. The authors have asked how glutamatergic neurons of the lateral horn respond to odors, i.e., whether they selectively encode odor identity, from which projection neurons they receive input, and whether a correlation between spatial response "pattern" and behavioral valence exists. Using state-of-the-art methods they demonstrate that, indeed, odor representations across …
Reviewer #2 (Public Review):
The fruit fly represents an excellent model organism to analyze in detail how odor stimuli are processed by brain circuits at different levels of complexity. Whereas much insight has been gained in recent years about peripheral processes at the level of sensory neurons and the primary circuits within the antennal lobes, the roles and interplay of the many and diverse neurons at higher brain levels such as the lateral horn remain less clear. The authors have asked how glutamatergic neurons of the lateral horn respond to odors, i.e., whether they selectively encode odor identity, from which projection neurons they receive input, and whether a correlation between spatial response "pattern" and behavioral valence exists. Using state-of-the-art methods they demonstrate that, indeed, odor representations across these neurons are odor-selective, and that the responses correlate with the atractiveness of the odor. Moreover, inhibitory and excitatory inputs from two antagonistically acting populations of projection neurons appear to shape the response patterns and contribute to the generation of such a valence code.
The experiments are excellently documented, the approaches are convincing and modern, the statistical analyses are sound and the manuscript is very clearly written. The overall conclusions are convincing and add an important point to our understanding of the olfactory pathway. I congratulate the authors to this excellent study and their interesting findings.
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Reviewer #3 (Public Review):
The lateral horn comprises multiple types of neurons, including a large fraction of glutamatergic neurons. This work investigates by functional imaging the general response properties of these glutamatergic neurons to odours of different valence. Complementing previous work, they find a certain degree of spatial stereotypy of response to odours and a correlation between amplitude of response of LH glutamatergic neurons and odour valence, which is not simply derived by the uPN input pattern. This is a solid piece of work improving our understanding of odour representation. The specific role of uPNs and iPNS in defining odour valence could be strengthened by an increased number of odours used.
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