Visual pursuit behavior in mice maintains the pursued prey on the retinal region with least optic flow

  1. Carl D Holmgren
  2. Paul Stahr
  3. Damian J Wallace
  4. Kay-Michael Voit
  5. Emily J Matheson
  6. Juergen Sawinski
  7. Giacomo Bassetto
  8. Jason ND Kerr  Is a corresponding author
  1. Department of Behavior and Brain Organization, Research center caesar, Germany
  2. Machine Learning in Science, Eberhard Karls University of Tübingen, Germany
7 figures, 6 videos, 5 tables and 1 additional file

Figures

Figure 1 with 1 supplement
Reconstruction of experimental arena and surrounds from the animal’s perspective.

(A) Schematic of experimental arena with olfactory and auditory noise. (B) Schematic of tracking, anatomical and eye camera calibration. Head position and orientation was tracked using seven IR-LEDs …

Figure 1—figure supplement 1
Generation of mouse eye views during cricket pursuit.

(A) Head pitch (red), roll (blue) and yaw (orange) and associated left (blue) and right (green) horizontal, vertical and torsional eye movements during the 46.2 s, example cricket pursuit sequence …

Figure 2 with 1 supplement
Mice use a focal region of their visual field to track prey.

(A) Mouse (black) and cricket (orange) paths during a single pursuit sequence (left), and for all pursuit sequences in one session for one animal (right). Pursuit start denoted as filled circles and …

Figure 2—figure supplement 1
Individual corneal prey image heatmaps.

(A) Probability density maps for detect (upper row) and track (lower row) epochs for each of the three animals individually. Data from 4 detect and 5 track sequences, 27 detect and 28 track …

Figure 3 with 1 supplement
Functional foci are not sampled by the highest density retinal ganglion cell region.

(A) Schematic of mouse eye model (left upper) with profile of all refractive indices (RI, left lower). Reconstructions of the optic disc (black), highest (>8000 cells/mm2, beige) and second highest …

Figure 3—figure supplement 1
Projecting high retinal ganglion cell density region from retina to cornea.

(A) Retinal whole mount redrawn from Dräger and Olsen, 1981 including whole mount outline (black), and outlines of the optic disc (black) and highest (>8000 cells/mm2, beige) and second highest (>700…

Figure 4 with 3 supplements
Functional foci are located within binocular regions in which motion is stabilized.

(A) Schematic of the common head and eye rotational axes. (B) Relationship between head and eye rotations around the common X (left, 154,625 frames from three animals) and Y (right, 165,432 frames …

Figure 4—figure supplement 1
VOR relationships between head and eye rotations and abrupt shifts in gaze.

VOR relationships between head and eye rotations and alignment of left and right eyes. (A) Relationship between mouse head pitch and horizontal eye rotations (left eye (171,942 frames), blue; right …

Figure 4—figure supplement 2
Ocular torsion during cricket pursuit.

(A) Distribution of left (blue) and right (green) eye torsional rotations during detect epochs. Data from 57 epochs (4406 frames) from three animals. (B) Distribution of ocular torsion during track …

Figure 4—figure supplement 3
VOR relationships between head and eye rotations and alignment of left and right eyes.

(A) Image of mouse with detachable miniaturized eye cameras and head position tracking system. (B) Example eye images showing horizontal, vertical and torsional eye rotations. Note TiO2 spots on the …

Figure 5 with 1 supplement
Mechanisms used to maintain prey within a focal visual region.

(A) Corneal locations of cricket position color-coded by Euclidean distance to cricket for non-track (upper) and track (lower) epochs (18 data sequences, 15649 non-tracking and 8510 tracking frames, …

Figure 5—figure supplement 1
Eye movements during non-tracking and tracking periods.

(A) Violin plots showing the variability in horizontal eye rotations for left (blue) and right (green) eyes during non-tracking (Non-trk) and track (Track) epochs. (B) Variability in vertical eye …

Functional foci are located in the regions of reduced optic flow during forward motion.

(A) Schematic of idealized optic flow (black arrows) as a mouse translates forwards (after Sabbah et al., 2017). Left (blue arrow) and right (green arrow) gaze vectors. (B) Location of optic flow …

Methods.

(A) Implanted baseplate with magnetic attachment point and restraining pin holes. (B) Miniaturized eye cameras and head position tracking system. Infrared illumination LEDs were mounted on the …

Videos

Video 1
Digitized and rendered view of the experiment arena and surrounding environment.

Laser scanned and digitally reconstructed experiment environmental, providing positional information of objects within the mouse’s environment. When combined with the tracked 3D cricket positions …

Video 2
Reconstruction of the mouse’s left and right eye field of view during one example behavioral sequence.

Real speed.

Video 3
Reconstruction of the mouse’s left and right eye field of view during one example behavioral sequence, as shown in Video 2, but slowed to 0.5x real speed.
Video 4
Left and right eye camera images and one overhead camera view showing one complete cricket pursuit, from shortly after release of the cricket into the arena to cricket capture.

Real Speed.

Video 5
The same cricket pursuit as shown in Video 4 but slowed to 0.5x real speed.
Video 6
Reconstructed left and right mouse-eye views for one example pursuit behavioral sequence, showing the trajectory of the cricket position in the eye views during the detect (red) and track (blue) segments of the behavior.

Tables

Table 1
Mouse eye model curvatures.

Radii of curvature of the optical components of the mouse eye model in Figure 3A.

Ocular ComponentRadius of curvature (μm)
Anterior Cornea−1408*
Posterior Cornea−1372*
Anterior Lens1150*
Posterior Lens1134*
Retina1598*
  1. * Values from Barathi et al., 2008.

Table 2
Mouse eye model thicknesses and refractive indices.
Ocular ComponentThickness(μm)Index of refraction
Cornea92*1.402*
Anterior chamber278*1.334*
Lens2004*1.36–1.55
Vitreous chamber609*1.333*
  1. * Values from Barathi et al., 2008.

    † Minimum and maximum values after eye model optimization.

Table 3
Compensation gain of eye rotations for head X or Y-axis rotations.

Effect of digitally freezing torsional, vertical, and horizontal eye rotations on the gain of compensation of X and Y head rotations. Data taken from 168,852 frames, from three animals.

EyeRotation directionRotationAll Rotations
(mean ± SD)
Eye rotation frozen
(mean ± SD)
LeftXTorsion−0.45 ± 0.12−0.24 ± 0.1
Horizontal−0.45 ± 0.12−0.32 ± 0.06
Vertical−0.45 ± 0.12−0.35 ± 0.08
RightXTorsion−0.48 ± 0.06−0.24 ± 0.01
Horizontal−0.48 ± 0.06−0.36 ± 0.08
Vertical−0.48 ± 0.06−0.34 ± 0.03
LeftYTorsion−0.51 ± 0.12−0.35 ± 0.05
Horizontal−0.51 ± 0.12−0.51 ± 0.11
Vertical−0.51 ± 0.12−0.16 ± 0.14
RightYTorsion−0.62 ± 0.05−0.45 ± 0.05
Horizontal−0.62 ± 0.05−0.62 ± 0.02
Vertical−0.62 ± 0.05−0.17 ± 0.03
Table 4
Eye rotations during non-tracking and tracking periods.

Horizontal, vertical, and torsional eye rotations during the non-tracking and tracking periods in Figure 5. Data taken from 18 non-track epochs and 18 track epochs, from three animals.

Ocular RotationNon-Trk
(mean ± SD) (median)
Track
(mean ± SD) (median)
p value (KS)P value (Student
T-test)
Lt Horizontal−1.8 ± 9.9°
(−1.7°)
−1.8 ± 14.9°
(−3.5°)
3.9x10−20.162
Lt Vertical0.8 ± 11.2°
(−0.4°)
4.5 ± 11.1°
(4.9°)
0.4250.616
Lt Torsional2.9 ± 16.1°
(0.0°)
1.3 ± 20.6°
(0.0°)
0.9450.610
Rt Horizontal5.7 ± 10.9°
(5.5°)
1.0 ± 9.9°
(1.7°)
9.82x10−21.08x10−2
Rt Vertical−3.6 ± 13.4°
(−6.3°)
5.6 ± 12.7°
(−7.1°)
0.9450.804
Rt Torsional0.32 ± 13.5°
(0.0°)
0.7 ± 12.3°
(0.0°)
0.4250.366
Key resources table
Reagent type (species) or resourceDesignationSource or referenceIdentifiersAdditional information
Software, algorithmMatlabMathworksMatlab 2019b
Software, algorithmOpenJDKOracleVersion 1.8.0_292
Software, algorithmCudaNvidiaRelease 10.1, V10.1.243
Software, algorithmPythonPython Software FoundationPython 3.8.10
Software, algorithmQtQt ProjectQmake 3.1, Qt 5.9.5
Software, algorithmOpenGLKhronos Group/Nvidia/AMDVersion 4.6.0

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