Drosophila gustatory projections are segregated by taste modality and connectivity
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Evaluation Summary:
The authors reconstructed the axons of gustatory receptor neurons from the labellum in an EM volume of a whole adult Drosophila brain. The authors were able to correlate the EM data with light microscopic data in terms of the identity of neurons reconstructed, thus enabling the use of published functional data already available in terms of different taste modalities. This revealed that extensive synaptic connections are found between neurons of the same modality. This paper will be of interest to neuroscientists working in the field of circuits and behavior, especially feeding behavior.
(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 agreed to share their name with the authors.)
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Abstract
Gustatory sensory neurons detect caloric and harmful compounds in potential food and convey this information to the brain to inform feeding decisions. To examine the signals that gustatory neurons transmit and receive, we reconstructed gustatory axons and their synaptic sites in the adult Drosophila melanogaster brain, utilizing a whole-brain electron microscopy volume. We reconstructed 87 gustatory projections from the proboscis labellum in the right hemisphere and 57 from the left, representing the majority of labellar gustatory axons. Gustatory neurons contain a nearly equal number of interspersed pre- and postsynaptic sites, with extensive synaptic connectivity among gustatory axons. Morphology- and connectivity-based clustering revealed six distinct groups, likely representing neurons recognizing different taste modalities. The vast majority of synaptic connections are between neurons of the same group. This study resolves the anatomy of labellar gustatory projections, reveals that gustatory projections are segregated based on taste modality, and uncovers synaptic connections that may alter the transmission of gustatory signals.
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Evaluation Summary:
The authors reconstructed the axons of gustatory receptor neurons from the labellum in an EM volume of a whole adult Drosophila brain. The authors were able to correlate the EM data with light microscopic data in terms of the identity of neurons reconstructed, thus enabling the use of published functional data already available in terms of different taste modalities. This revealed that extensive synaptic connections are found between neurons of the same modality. This paper will be of interest to neuroscientists working in the field of circuits and behavior, especially feeding behavior.
(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 agreed to share their name with the …
Evaluation Summary:
The authors reconstructed the axons of gustatory receptor neurons from the labellum in an EM volume of a whole adult Drosophila brain. The authors were able to correlate the EM data with light microscopic data in terms of the identity of neurons reconstructed, thus enabling the use of published functional data already available in terms of different taste modalities. This revealed that extensive synaptic connections are found between neurons of the same modality. This paper will be of interest to neuroscientists working in the field of circuits and behavior, especially feeding behavior.
(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 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
Engert et al. provides a nearly complete synaptic level description of the anatomy of gustatory receptor neurons (GRNs), reveals their connectivity, and shows that they segregate based on taste modality. They find that pre and post-synaptic sites are distributed along the axons of all GRNs, as well as that each GRN receives synaptic inputs from other GRNs. Using hierarchical clustering Engert et al. defined six GRN classes based on their distinct morphology and connectivity. Next, they matched the anatomy of the six classes to the anatomy of known GRN classes that detect different taste modalities. They reveal that GRNs of each class are highly connected with each other, as well as weaker connected between different classes. Therefore, the authors performed calcium and voltage imaging to elucidate the role …
Reviewer #1 (Public Review):
Engert et al. provides a nearly complete synaptic level description of the anatomy of gustatory receptor neurons (GRNs), reveals their connectivity, and shows that they segregate based on taste modality. They find that pre and post-synaptic sites are distributed along the axons of all GRNs, as well as that each GRN receives synaptic inputs from other GRNs. Using hierarchical clustering Engert et al. defined six GRN classes based on their distinct morphology and connectivity. Next, they matched the anatomy of the six classes to the anatomy of known GRN classes that detect different taste modalities. They reveal that GRNs of each class are highly connected with each other, as well as weaker connected between different classes. Therefore, the authors performed calcium and voltage imaging to elucidate the role of the low-level connectivity of different GRN classes with each other. Interestingly, no crosstalk between the different classes could be detected.
The data are appropriately controlled and analyzed and support the conclusions drawn in this paper.
Strength
This manuscript provides the first nearly complete synaptic level description of gustatory receptor neurons. Given that the authors reconstructed GRNs in the FAFB electron microscopy dataset manually or using a combination of automated segmentation and manual tracing using Catmaid, the synapse numbers presented here are all verified and trustworthy.The authors went to great lengths to test every possible synaptic connection between different GRN classes using calcium and voltage imaging. Unfortunately, no mechanism for the alteration of the transmission of gustatory signals between different GRN classes was uncovered yet, however, it shows that it is extremely important to test the functionality of synapses seen in EM datasets.
Weaknesses
Given that manual tracing in Catmaid is very time-consuming it is difficult to complete the entire population of GRNs and be competitive with similar work being performed using other EM platforms with automated segmentation. Therefore, the authors could not determine how large the actual GRN population is and whether there might be additional unknown classes. -
Reviewer #2 (Public Review):
This paper utilizes the whole brain EM volume of the adult Drosophila to elucidate the synaptic connectivity patterns of the gustatory sensory neurons in the brain. The reconstruction is focused on the gustatory sensory axons of the labial nerve, which houses sensory axons from the labellum, maxillary palp and the eye, as well as motor axons that innervate the proboscis. The labellar gustatory axons terminate in specific regions of the SEZ termed the anterior central sensory center (ACSC). 87 projections were reconstructed on the right side (representing 83-96% of the total estimated); 57 projections were done for the left side (54-63% total), attributed to registration error in the volume. Morphological and synaptic clustering led to the identification of 6 different regions/zones in the ACSC on which the …
Reviewer #2 (Public Review):
This paper utilizes the whole brain EM volume of the adult Drosophila to elucidate the synaptic connectivity patterns of the gustatory sensory neurons in the brain. The reconstruction is focused on the gustatory sensory axons of the labial nerve, which houses sensory axons from the labellum, maxillary palp and the eye, as well as motor axons that innervate the proboscis. The labellar gustatory axons terminate in specific regions of the SEZ termed the anterior central sensory center (ACSC). 87 projections were reconstructed on the right side (representing 83-96% of the total estimated); 57 projections were done for the left side (54-63% total), attributed to registration error in the volume. Morphological and synaptic clustering led to the identification of 6 different regions/zones in the ACSC on which the axons terminate. Critically, and this is the really great part of this work, the authors were able to correlate the EM data with light microscopic data in terms of the identity of neurons reconstructed, thus enabling the use of published functional data already available in terms of different taste modalities. This revealed that extensive synaptic connections are found between neurons of the same modality. The functional analysis further showed that activation of neurons of one modality does not affect those of others.
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