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

  1. Timothy A Currier
  2. Andrew MM Matheson
  3. Katherine I Nagel  Is a corresponding author
  1. Neuroscience Institute, New York University Langone Medical Center, United States
  2. Center for Neural Science, New York University, United States
8 figures, 2 tables and 1 additional file

Figures

Figure 1 with 3 supplements
Sensory responses and preferred airflow direction vary across CX columnar cell types.

(A) Experimental preparation. We targeted single neurons for patching using cell type-specific expression of GFP. Flies were placed in an arena equipped with rotatable stimulus delivery and live …

Figure 1—figure supplement 1
Baseline activity characterization for recorded cell types.

(A) CX neuropils innervated by each recorded cell type. Each cell type is named after standard nomenclature: single letters represent innervated neuropil (gray), with putative input regions before …

Figure 1—figure supplement 2
Summary of sensory responses across CX cell types.

(A) CX neuropils innervated by each recorded cell type. (B) Maximal responses to each stimulus condition. Gray dots represent the mean absolute spiking response of each cell to four presentations …

Figure 1—figure supplement 3
Tuned visual responses in E-PGs.

(A) Top: neuropil schematic of E-PG (‘compass’) neurons, which are known to be tuned for both visual landmark orientation (Green et al., 2017) and airflow direction (Okubo et al., 2020). Bottom: …

Figure 2 with 1 supplement
CX columnar neurons sum inputs from different modalities on average, but show diverse integration strategies at the level of single cells.

(A) Summation of multimodal cues. Left: mean spiking response to stripe and airflow together versus sum of mean stripe alone and airflow alone responses. Each point represents the response of one …

Figure 2—figure supplement 1
Characterization of multi-sensory integration for recorded cell types.

Each plot shows the similarity (correlation coefficient) of the response to airflow + stripe with the response to airflow alone (y-axis) versus stripe alone (x-axis), as in Figure 2 and 3. Each …

Ventral P-FNs selectively respond to directional airflow.

(A) Left: CX neuropils innervated by P-F2N3. Right: color key for directional stimuli. (B) Example trials from a single P-F2N3 neuron. Raw membrane potential for single presentations of airflow …

Ventral P-FNs exhibit similar ipsilateral airflow tuning across CX columns.

(A) Top: CX neuropils innervated by P-F2N3. Bottom: experimental setup. We presented airflow from eight directions and identified the column innervated by each patched neuron by filling the cell …

Figure 5 with 1 supplement
LNa neurons are a likely source of airflow signals in ventral P-FNs.

(A) Experimental framework. Neurons with tuned airflow responses have recently been identified in the Antler (ATL) and Lateral Accessory Lobe (LAL). We recorded from vFBN (green) and LNa (orange) …

Figure 5—figure supplement 1
Trans-tango of VT029515 (vFBN).

P-FNs are putatively downstream of VT029515 neurons (vFBNs). vFBNs (green) receive input in the Antler (Ant) and project to layer 2 of the FB. Trans-tango signal (magenta) can be seen in all …

Figure 6 with 1 supplement
Silencing ventral P-FNs disrupts orientation to airflow.

(A) Schematic of flight simulator arena. Rigidly tethered flying flies orient in closed-loop with an airflow stream. Infrared illumination is used to track wingbeat angles which drive airflow …

Figure 6—figure supplement 1
Full central brain anatomy of R44B10-GAL4.

Little GFP expression can be seen outside of the CX in R44B10-GAL4. Weak off-target signal is present in the mushroom bodies (MB), ventrolateral protocerebrum (VLP), and sub-esophageal zone (SEZ). …

R44B10 neurons are required to convert airflow orientation changes into heading-appropriate turns.

(A) Stimulus manipulations. Six manipulations were presented pseudo-randomly every 20 s during closed-loop flight: long wind pause (2 s); short wind pause (150 msec); short (14.44°) and long …

Airflow-representing circuits in the CX.

Airflow direction is transduced via antennal deflection signals (purple), which are transmitted through the AMMC and Wedge to the LAL (Yorozu et al., 2009; Suver et al., 2019; Okubo et al., 2020). A …

Tables

Table 1
Intrinsic properties of surveyed neuron types.
Cell typeDriver lineNResting potential (mV)Input resistance (GΩ)Osc. freq. (Hz)
P-F1N3SS522446−18.0 ± 1.06.21 ± 0.524
P-F2N3SS022556−22.0 ± 1.34.86 ± 0.502
P-F3N2dSS0007814−30.9 ± 0.92.58 ± 0.24-
P-F3N2vSS525774−31.8 ± 3.56.00 ± 0.50-
P-EN1SS542954−32.9 ± 2.12.52 ± 0.293
P-EN2R12D096−30.1 ± 1.93.30 ± 0.293
P-F3LCSS022398−39.7 ± 0.82.75 ± 1.11-
P-F3-5RSS545496−26.3 ± 1.37.89 ± 0.51-
E-PGSS000904−29.4 ± 1.52.30 ± 0.35-
  1. Resting potential, input resistance, and characteristic oscillatory frequency are shown for each recorded cell type. Values represent the cross-fly mean +/- SEM. See also Figure 1—figure supplement 1.

Key resources table
Reagent type (species) or resourceDesignationSource or referenceIdentifiersAdditional information
Genetic reagent (D. melanogaster)SS52244-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_86596
Genetic reagent (D. melanogaster)SS02255-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_75923
Genetic reagent (D. melanogaster)SS00078-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_75854
Genetic reagent (D. melanogaster)SS52577-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_86625
Genetic reagent (D. melanogaster)SS54295-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_86624
Genetic reagent (D. melanogaster)SS02239-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_75926
Genetic reagent (D. melanogaster)SS54549-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_86603
Genetic reagent (D. melanogaster)SS47432-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_86716
Genetic reagent (D. melanogaster)R12D09-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_48503
Genetic reagent (D. melanogaster)R44B10-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_50202
Genetic reagent (D. melanogaster)(empty)-GAL4Bloomington Drosophila Stock CenterRRID:BDSC_68384
Genetic reagent (D. melanogaster)10xUAS-IVS-syn21-GFP-p10 (attP2)Michael DickinsonN/A
Genetic reagent (D. melanogaster)13xUAS-Kir2.1-eGFP/TM3Michael ReiserN/A
Genetic reagent (D. melanogaster)20xUAS-GCaMP6fBloomington Drosophila Stock CenterRRID:BDSC_42747
Genetic reagent (D. melanogaster)UAS-tdTomatoBloomington Drosophila Stock CenterRRID:BDSC_36328
Antibody(mouse monoclonal) anti-NC82Developmental Studies Hybridoma BankRRID:AB_2314866(1:50)
Antibody(chicken polyclonal) anti-GFPThermo Fisher ScientificPA1-9533(1:50)
Antibodystreptavidin Alexa Fluor 568Thermo Fisher ScientificS-11226(1:1000)
Antibody(goat polyclonal) anti-mouse Alexa Fluor 633Thermo Fisher ScientificA-21052(1:250)
Antibody(goat polyclonal) anti-chicken Alexa Fluor 488Thermo Fisher ScientificA-11039(1:250)

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