Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat

  1. Ninad B Kothari
  2. Melville J Wohlgemuth
  3. Cynthia F Moss  Is a corresponding author
  1. Johns Hopkins University, United States
6 figures, 2 videos and 2 additional files

Figures

Figure 1 with 3 supplements
Experimental setup and methodology.

(A) Configuration of the experimental flight room for wireless, chronic neural recordings from freely flying echolocating bats. Shown is the bat (in brown) with the neural telemetry device mounted …

https://doi.org/10.7554/eLife.29053.003
Figure 1—figure supplement 1
Cross-correlation of flight paths.

(A) Trial-by-trial cross correlations of flight paths for Bat 1, showing the XY projection. The autocorrelation of the same trial is shown along the diagonal. Letters at the top indicate different …

https://doi.org/10.7554/eLife.29053.004
Figure 1—figure supplement 2
Spike waveform consistency throughout a single recording session.

(A) Top, all data from a single channel from a single recording session. Spikes and movement artifact are indicated. Bottom, time expanded portions of the beginning (blue), middle (red), and end …

https://doi.org/10.7554/eLife.29053.005
Figure 1—figure supplement 3
Spike cluster separation.

Shown are the Lratio data for all clusters as determined by the wavelet-based clustering algorithm use to sort spikes.

https://doi.org/10.7554/eLife.29053.006
Figure 2 with 2 supplements
Use of the echo model to determine the bat’s ongoing sensory signal reception.

(A) Cartoon of a bat flying through space encountering two obstacles. The bat’s flight trajectory moves from right to left, and is indicated by the black dotted line. Two sonar vocalizations while …

https://doi.org/10.7554/eLife.29053.007
Figure 2—figure supplement 1
Head aim reconstruction.

(A) Cartoon of the bat with the TBSI telemetry head-stage (grey box), and the Omnetics connectors (brown boxes), which connect the head-stage with the plug on the bat’s head. (B) Top view of the …

https://doi.org/10.7554/eLife.29053.008
Figure 2—figure supplement 2
Error analysis and validation of the echo-model.

(A) Cross-section of the cylindrical object placed along the flight path of the object. The height and radius of the object are 10 cm and 6 cm respectively. P is an example point in the trajectory …

https://doi.org/10.7554/eLife.29053.009
Figure 3 with 2 supplements
Range tuning of midbrain neurons.

(A) A cartoon representation showing the target range estimation in a free-flying echolocating bat. The difference between the call production time (T0, red arrow) and the echo arrival time (TE, …

https://doi.org/10.7554/eLife.29053.010
Figure 3—figure supplement 1
Spatial coverage during the experiment.

(A) Flight paths (black lines), vocalizations (yellow dots) and obstacles (pink circles) for one recording session. (B) Histogram of calls per recording session. (C) Histogram of number of echoes …

https://doi.org/10.7554/eLife.29053.011
Figure 3—figure supplement 2
Spatial tuning in azimuth and elevation.

(A) Histogram of azimuthal tuning for the neuron in Figure 3B. Inset is a polar-plot representation of azimuthal tuning. (B) Histogram of elevation tuning for the neuron in panel Figure 3B. Inset is …

https://doi.org/10.7554/eLife.29053.012
Figure 4 with 3 supplements
Spatial tuning of neurons recorded in the SC.

(A) Egocentric locations of echo sources eliciting activity from a single SC neuron. Red dots indicate echo source locations eliciting spikes, black dots indicate echo source locations where a spike …

https://doi.org/10.7554/eLife.29053.013
Figure 4—figure supplement 1
Stability of distance tuning across the first and last half of each recording session.

Shows the comparison of peak distance tuning of neurons (n = 37) for the first and second half of each recording session. Dots in red indicate neurons which show significant change in distance …

https://doi.org/10.7554/eLife.29053.014
Figure 4—figure supplement 2
Changes in depth tuning as a function of recording depth.

CIslope indicates the 95% confidence interval of the slope fitted using bootstrapping.

https://doi.org/10.7554/eLife.29053.015
Figure 4—figure supplement 3
Distribution of cells showing 3D, 2D and 1D spatial tuning.

Out of the 67 sensory neurons (see criterion above), overlapping populations of neurons showed either 3D, 2D or 1D spatial selectivity. 46 neurons showed spatial selectivity in 3D (azimuth, …

https://doi.org/10.7554/eLife.29053.016
Figure 5 with 1 supplement
Adaptive vocal behavior drives changes in spatial tuning of SC neurons.

(A) Three-dimensional view of one flight path (in black) through the experimental room. Individual sonar vocalizations that are not included in a sonar sound group (non-SSG) are shown as blue …

https://doi.org/10.7554/eLife.29053.017
Figure 5—figure supplement 1
Changes in firing probability and spatial receptive fields for the first and last call of SSGs.

(A) Shows the percentage increase in firing probability (y-axis) for every 3D tuned neuron (x-axis, n = 46). Panel on the right shows the summary box plot of the distribution of the same data in the …

https://doi.org/10.7554/eLife.29053.018
Figure 6 with 2 supplements
Increases in gamma power correlate with sonar-guided spatial attention.

(A) Schematic of sonar sound group (SSG) determination. SSG’s are identified by brief epochs of higher vocal rate (i.e. shorter interval in red) surrounded by vocalizations at a lower rate (i.e. …

https://doi.org/10.7554/eLife.29053.019
Figure 6—figure supplement 1
Changes in gamma band power ratio for SSG and non-SSGs with recording depth.

CIslope indicates the 95% confidence interval of the slope fitted using bootstrapping.

https://doi.org/10.7554/eLife.29053.020
Figure 6—figure supplement 2
Wing beat motion artifact in LFP.

The x-axis is the ratio of power in the low frequency (10–20 Hz) LFP band to the gamma LFP band in dB.

https://doi.org/10.7554/eLife.29053.021

Videos

Video 1
Experimental setup for validating the echo model.

This is a two-part movie. The first part shows the layout of the microphone array, which is used to capture the sonar vocalizations of the bat as it flies and navigates around objects in its path. …

https://doi.org/10.7554/eLife.29053.022
Video 2
Validation of echo model using time-difference-of-arrival (TDOA) algorithms.

This is a two-part movie. The first part consists of 3 panels. The top panel shows an example trajectory as the bat navigates across objects (white and green). The red line is the reconstructed …

https://doi.org/10.7554/eLife.29053.023

Additional files

Supplementary file 1

(A) Comparison of the variance of SSG and non-SSG distance tuning distributions for each cell in Figure 5D.

The SSG and non-SSG distance tuning distributions were compared using the non-parametric Brown-Forsythe Test at the level α of 0.05. Cells in red show a significant sharpening in the distance tuning distribution when the bat emitted SSGs as compared to the variance of the distance tuning distribution when the bat produced single calls (non-SSGs). Cells in gray did not show a significant effect. Cells in blue showed a significant effect but in the opposite direction. (B) Comparison of the SSG and non-SSG distance tuning distributions for each cell in Figure 5F. The SSG and non-SSG distance tuning distributions were compared using the non-parametric Wilcoxon Rank Sum Test at an α of 0.05. Cells marked with red ink show a significant shortening in distance tuning for SSGs as compared to the condition when the bat produces single calls (non-SSGs). Cells marked with gray ink did not show a significant effect.

https://doi.org/10.7554/eLife.29053.024
Transparent reporting form
https://doi.org/10.7554/eLife.29053.025

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