Encoding and control of orientation to airflow by a set of Drosophila fan-shaped body neurons
Abstract
The insect Central Complex (CX) is thought to underlie goal-oriented navigation but its functional organization is not fully understood. We recorded from genetically-identified CX cell types in Drosophila and presented directional visual, olfactory, and airflow cues known to elicit orienting behavior. We found that a group of neurons targeting the ventral fan-shaped body (ventral P-FNs) are robustly tuned for airflow direction. Ventral P-FNs did not generate a 'map' of airflow direction. Instead, cells in each hemisphere were tuned to 45° ipsilateral, forming a pair of orthogonal bases. Imaging experiments suggest that ventral P-FNs inherit their airflow tuning from neurons that provide input from the lateral accessory lobe (LAL) to the noduli (NO). Silencing ventral P-FNs prevented flies from selecting appropriate corrective turns following changes in airflow direction. Our results identify a group of central complex neurons that robustly encode airflow direction and are required for proper orientation to this stimulus.
Data availability
All electrophysiology, behavior, and anatomy data are publicly available on Dryad at https://doi.org/10.5061/dryad.vq83bk3rh.
-
Encoding and control of airflow orientation by a set of Drosophila fan-shaped body neuronsDryad Digital Repository, doi:10.5061/dryad.vq83bk3rh.
-
A connectome of the Adult Drosophila Central Braindoi: https://doi.org/10.1101/2020.01.21.911859.
-
neuPrint: Analysis Tools for EM Connectomicsdoi: https://doi.org/10.1101/2020.01.16.909465.
Article and author information
Author details
Funding
National Institute on Deafness and Other Communication Disorders (R01DC017979)
- Katherine I Nagel
National Institute of Mental Health (R01MH109690)
- Katherine I Nagel
McKnight Endowment Fund for Neuroscience (Scholar Award)
- Katherine I Nagel
National Science Foundation (IOS-1555933)
- Katherine I Nagel
New York University (Dean's Fellowship)
- Timothy A Currier
National Science Foundation (neuronex)
- Katherine I Nagel
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Ronald L Calabrese, Emory University, United States
Version history
- Received: July 28, 2020
- Accepted: December 29, 2020
- Accepted Manuscript published: December 30, 2020 (version 1)
- Version of Record published: January 8, 2021 (version 2)
Copyright
© 2020, Currier et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,096
- views
-
- 423
- downloads
-
- 46
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
The brain’s ability to appraise threats and execute appropriate defensive responses is essential for survival in a dynamic environment. Humans studies have implicated the anterior insular cortex (aIC) in subjective fear regulation and its abnormal activity in fear/anxiety disorders. However, the complex aIC connectivity patterns involved in regulating fear remain under investigated. To address this, we recorded single units in the aIC of freely moving male mice that had previously undergone auditory fear conditioning, assessed the effect of optogenetically activating specific aIC output structures in fear, and examined the organization of aIC neurons projecting to the specific structures with retrograde tracing. Single-unit recordings revealed that a balanced number of aIC pyramidal neurons’ activity either positively or negatively correlated with a conditioned tone-induced freezing (fear) response. Optogenetic manipulations of aIC pyramidal neuronal activity during conditioned tone presentation altered the expression of conditioned freezing. Neural tracing showed that non-overlapping populations of aIC neurons project to the amygdala or the medial thalamus, and the pathway bidirectionally modulated conditioned fear. Specifically, optogenetic stimulation of the aIC-amygdala pathway increased conditioned freezing, while optogenetic stimulation of the aIC-medial thalamus pathway decreased it. Our findings suggest that the balance of freezing-excited and freezing-inhibited neuronal activity in the aIC and the distinct efferent circuits interact collectively to modulate fear behavior.
-
- Neuroscience
Motor learning is often viewed as a unitary process that operates outside of conscious awareness. This perspective has led to the development of sophisticated models designed to elucidate the mechanisms of implicit sensorimotor learning. In this review, we argue for a broader perspective, emphasizing the contribution of explicit strategies to sensorimotor learning tasks. Furthermore, we propose a theoretical framework for motor learning that consists of three fundamental processes: reasoning, the process of understanding action–outcome relationships; refinement, the process of optimizing sensorimotor and cognitive parameters to achieve motor goals; and retrieval, the process of inferring the context and recalling a control policy. We anticipate that this ‘3R’ framework for understanding how complex movements are learned will open exciting avenues for future research at the intersection between cognition and action.