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The conserved RNA-binding protein Imp is required for the specification and function of olfactory navigation circuitry in Drosophila

Hamid, Aisha; Gattuso, Hannah; Caglar, Aysu Nora; Pillai, Midhula; Steele, Theresa; Gonzalez, Alexa; Nagel, Katherine; Syed, Mubarak Hussain
Complex behaviors depend on the precise developmental specification of neuronal circuits, but the relationship between genetic programs for neural development, circuit structure, and behavioral output is often unclear. The central complex (CX) is a conserved sensory-motor integration center in insects, which governs many higher-order behaviors and largely derives from a small number of type II neural stem cells (NSCs). Here, we show that Imp, a conserved IGF-II mRNA-binding protein expressed in type II NSCs, plays a role in specifying essential components of CX olfactory navigation circuitry. We show the following: (1) that multiple components of olfactory navigation circuitry arise from type II NSCs. (2) Manipulating Imp expression in type II NSCs alters the number and morphology of many of these circuit elements, with the most potent effects on neurons targeting the ventral layers of the fan-shaped body (FB). (3) Imp regulates the specification of Tachykinin-expressing ventral FB input neurons. (4) Imp is required in type II NSCs for establishing proper morphology of the CX neuropil structures. (5) Loss of Imp in type II NSCs abolishes upwind orientation to attractive odor while leaving locomotion and odor-evoked regulation of movement intact. Taken together, our findings establish that a temporally expressed gene can regulate the expression of a complex behavior by developmentally regulating the specification of multiple circuit components and provides a first step toward a developmental dissection of the CX and its roles in behavior.
PMID: 38181792
ISSN: 1879-0445
CID: 5633142

Astrocyte growth is driven by the Tre1/S1pr1 phospholipid-binding G protein-coupled receptor

Chen, Jiakun; Stork, Tobias; Kang, Yunsik; Nardone, Katherine A M; Auer, Franziska; Farrell, Ryan J; Jay, Taylor R; Heo, Dongeun; Sheehan, Amy; Paton, Cameron; Nagel, Katherine I; Schoppik, David; Monk, Kelly R; Freeman, Marc R
Astrocytes play crucial roles in regulating neural circuit function by forming a dense network of synapse-associated membrane specializations, but signaling pathways regulating astrocyte morphogenesis remain poorly defined. Here, we show the Drosophila lipid-binding G protein-coupled receptor (GPCR) Tre1 is required for astrocytes to establish their intricate morphology in vivo. The lipid phosphate phosphatases Wunen/Wunen2 also regulate astrocyte morphology and, via Tre1, mediate astrocyte-astrocyte competition for growth-promoting lipids. Loss of s1pr1, the functional analog of Tre1 in zebrafish, disrupts astrocyte process elaboration, and live imaging and pharmacology demonstrate that S1pr1 balances proper astrocyte process extension/retraction dynamics during growth. Loss of Tre1 in flies or S1pr1 in zebrafish results in defects in simple assays of motor behavior. Tre1 and S1pr1 are thus potent evolutionarily conserved regulators of the elaboration of astrocyte morphological complexity and, ultimately, astrocyte control of behavior.
PMID: 38096817
ISSN: 1097-4199
CID: 5588882

Olfactory navigation in arthropods

Steele, Theresa J; Lanz, Aaron J; Nagel, Katherine I
Using odors to find food and mates is one of the most ancient and highly conserved behaviors. Arthropods from flies to moths to crabs use broadly similar strategies to navigate toward odor sources-such as integrating flow information with odor information, comparing odor concentration across sensors, and integrating odor information over time. Because arthropods share many homologous brain structures-antennal lobes for processing olfactory information, mechanosensors for processing flow, mushroom bodies (or hemi-ellipsoid bodies) for associative learning, and central complexes for navigation, it is likely that these closely related behaviors are mediated by conserved neural circuits. However, differences in the types of odors they seek, the physics of odor dispersal, and the physics of locomotion in water, air, and on substrates mean that these circuits must have adapted to generate a wide diversity of odor-seeking behaviors. In this review, we discuss common strategies and specializations observed in olfactory navigation behavior across arthropods, and review our current knowledge about the neural circuits subserving this behavior. We propose that a comparative study of arthropod nervous systems may provide insight into how a set of basic circuit structures has diversified to generate behavior adapted to different environments.
PMID: 36658447
ISSN: 1432-1351
CID: 5419252

SAMPL is a high-throughput solution to study unconstrained vertical behavior in small animals

Zhu, Yunlu; Auer, Franziska; Gelnaw, Hannah; Davis, Samantha N; Hamling, Kyla R; May, Christina E; Ahamed, Hassan; Ringstad, Niels; Nagel, Katherine I; Schoppik, David
Balance and movement are impaired in many neurological disorders. Recent advances in behavioral monitoring provide unprecedented access to posture and locomotor kinematics but without the throughput and scalability necessary to screen candidate genes/potential therapeutics. Here, we present a scalable apparatus to measure posture and locomotion (SAMPL). SAMPL includes extensible hardware and open-source software with real-time processing and can acquire data from D. melanogaster, C. elegans, and D. rerio as they move vertically. Using SAMPL, we define how zebrafish balance as they navigate vertically and discover small but systematic variations among kinematic parameters between genetic backgrounds. We demonstrate SAMPL's ability to resolve differences in posture and navigation as a function of effect size and data gathered, providing key data for screens. SAMPL is therefore both a tool to model balance and locomotor disorders and an exemplar of how to scale apparatus to support screens.
PMID: 37267107
ISSN: 2211-1247
CID: 5543482

Active antennal movements in Drosophila can tune wind encoding

Suver, Marie P; Medina, Ashley M; Nagel, Katherine I
Insects use their antennae to smell odors,1
PMID: 36731464
ISSN: 1879-0445
CID: 5420472

Olfaction: The smell stops here [Comment]

Nagel, Katherine
A recent study has shown that, in the fly Drosophila, olfactory neurons stop signaling when smells get too strong. This changes the way we think about odor encoding across concentrations.
PMID: 36854272
ISSN: 1879-0445
CID: 5448462

A neural circuit for wind-guided olfactory navigation

Matheson, Andrew M M; Lanz, Aaron J; Medina, Ashley M; Licata, Al M; Currier, Timothy A; Syed, Mubarak H; Nagel, Katherine I
To navigate towards a food source, animals frequently combine odor cues about source identity with wind direction cues about source location. Where and how these two cues are integrated to support navigation is unclear. Here we describe a pathway to the Drosophila fan-shaped body that encodes attractive odor and promotes upwind navigation. We show that neurons throughout this pathway encode odor, but not wind direction. Using connectomics, we identify fan-shaped body local neurons called h∆C that receive input from this odor pathway and a previously described wind pathway. We show that h∆C neurons exhibit odor-gated, wind direction-tuned activity, that sparse activation of h∆C neurons promotes navigation in a reproducible direction, and that h∆C activity is required for persistent upwind orientation during odor. Based on connectome data, we develop a computational model showing how h∆C activity can promote navigation towards a goal such as an upwind odor source. Our results suggest that odor and wind cues are processed by separate pathways and integrated within the fan-shaped body to support goal-directed navigation.
PMID: 35941114
ISSN: 2041-1723
CID: 5286712

Motion vision: Pinning down motion computation in an ever-changing circuit

Nagel, Katherine
A new electrophysiological study of the Drosophila visual system, recording from columnar inputs to motion-detecting neurons, has provided new insights into the computations that underlie motion vision.
PMID: 34875241
ISSN: 1879-0445
CID: 5110192

Encoding and control of orientation to airflow by a set of Drosophila fan-shaped body neurons

Currier, Timothy A; Matheson, Andrew Mm; Nagel, Katherine I
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 CX neurons that robustly encode airflow direction and are required for proper orientation to this stimulus.
PMID: 33377868
ISSN: 2050-084x
CID: 4771002

Experience- and Context-Dependent Modulation of the Invertebrate Compass System

Currier, Timothy A; Nagel, Katherine I
How are head direction signals computed and maintained in neural circuits? In this issue of Neuron, Shiozaki et al. (2020) expand our understanding of the fly "compass" network, revealing context- and experience-dependent changes in the multiplexed encoding of head direction and steering maneuvers.
PMID: 32272068
ISSN: 1097-4199
CID: 4379002