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Method Article

Non-aversive Animal Restraint Enabling Recording of Optomotor Reflex in Ground Squirrels

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DOI:

10.3791/68335

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July 25th, 2025

 ,  ,  ,  ,  , 
1Retinal Neurophysiology Section, National Eye Institute, National Institutes of Health, 2Department of Ophthalmology, Faculty of Medicine, University of Murcia and Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 3Striatech GmbH

In This Article

Summary

The protocol describes how to measure the optomotor response in 13-lined ground squirrels, a cone-dominant species with retinal features resembling the human macula. The platform design enhances handling and reduces anxiety, improving the animal's ability to stay on the raised platform, enabling non-invasive assessment of changes in visual function.

Abstract

The optomotor reflex (OMR) provides a behavioral assessment of an animal's contrast sensitivity and visual acuity. Mice or rats are typically placed directly onto a small circular platform by hand; however, handling animals like this can stimulate stress and anxiety, which introduce confounding factors when interpreting data. It has been shown that non-aversive handling methods, such as picking up mice or rats in a familiar tunnel/tube, can reduce anxiety. This is of particular interest in studies where animals display heightened stress, overactivity, or motor dysfunction, resulting in an inability to stay on the platform. A team led by Drs. Kiyoharu J. Miyagishima and Francisco M. Nadal-Nicolás have redesigned the conventional OMR platform to provide semi-closed containment. This makes it possible for the first time to record the optomotor reflex in the 13-lined ground squirrel, which is one of the few mammals that can see color. It has a visual streak with a high density of cones similar to the human macula providing an attractive model for studying effects on the cone visual system.

Introduction

Ground squirrels offer a unique and valuable model for studying visual function due to their diurnal lifestyle and cone-dominated retinas, which closely mimic human vision1. This, coupled with the practical advantages of their use (smaller size, lower husbandry cost) compared to primates, make them an ideal model for translational research into retinal injury, disease, or ocular side effects of drugs on color vision changes2,3,4,5,6. Preclinical research on retinal diseases relies on the ability to assess whether an animal can see. The optomotor reflex (OMR) offers a clinically relevant method for evaluating visual function in animals without the need for anesthesia, enabling an accurate measurement of visual acuity7,8. In this test, the animal follows a rotating stripe pattern with its gaze. The rotating stripes induce the perception of global motion in the environment, triggering an involuntary head movement - the OMR. This reflex serves to visually stabilize the environment and can be used to quantify how well an animal can see by incrementally adjusting the spatial frequency or contrast of the stimulus. As the stimulus becomes more difficult to perceive, the OMR is eventually not triggered, allowing the determination of visual acuity or contrast threshold. The advantage of the OMR is that it is a reflex. Thus, no training is required, and head fixation or surgery is unnecessary. The reflex is present even in very young animals (upon eye-opening)9,10, making it possible to study early-onset diseases. Additionally, since it is noninvasive, longitudinal measurements can be made enabling tracking of disease progression.

Most OMR testing is performed using custom or commercial systems that consist of a raised platform where the animal is placed, surrounded by four screens displaying rotating black and white stripe patterns. The stripes move in one direction (clockwise or counterclockwise), creating a motion stimulus that elicits a visual tracking response from the animal10,11,12,13,14,15,16. A camera is mounted above the testing arena to capture the animal's visually evoked head movements in response to the rotating stimulus. These head movements are tracked and analyzed to determine the animal's ability to perceive and respond to motion, thereby assessing its visual acuity.

Although the OMR is routinely used in mice and rats, measurement of the optomotor response in 13-lined ground squirrels has been challenging due to their hyperactivity and inability to stay on elevated platforms, even with prior conditioning. To circumvent this, we developed a platform that provides semi-containment, facilitating the transfer of the animals to the arena. The goal of this method is to reduce the time for the animals to adapt to the experimental setting, enabling the recording of animals that display uncooperative behavior or have difficulty staying on the platform and improving the inclusion of animals in studies. We have also defined a protocol to measure visual acuity in squirrels using an experimentally defined contrast setting and have adjusted the camera settings for improved imaging results, enabling automated analysis and tracking.

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Protocol

The procedures involving animals were conducted in adherence to the laws of the United States and the regulations of the Department of Agriculture. All experiments with animals were conducted according to protocols approved by the Animal and Care and Use Committee of the National Eye Institute at the National Institutes of Health. Male and female 13-lined ground squirrels (ages 6-8 months) used in this study were purchased from the University of Wisconsin Oshkosh Squirrel Colony. Mice (rd10: 1 month, CX3CR1GFP/+: 6.5 months) used in this study were bred in our animal facility. Animals and their cages were randomly selected and assigned to experimental groups.

1. Preparation of the prototype platform and modified handling tunnel

NOTE: Round flat platforms are commonly employed in systems designed to measure the optomotor response13. However, hyperactive rodent models, such as squirrels, often struggle to maintain stability on these platforms. This design provides a semi-enclosed space, which helps the animals habituate quickly and reduces anxiety-like behaviors. This improvement enhances the animal's ability to focus and minimizes instances of imbalance or falls during recordings.

  1. In CAD drawing software (e.g., OpenSCAD or FreeCAD), design the platform (gray) and the enclosure (red) as shown in Figure 1.
    1. Ensure that the key dimensions for the squirrel platform are maintained as the length and width (L x W): 129 mm x 81 mm, the thickness: 7 mm, and the height of the wall that extends around the perimeter: 8 mm. Use the provided free CAD standard document file for the prototype platform (squirrel) used in this proof-of-concept study (Supplementary Coding File 1).
    2. Ensure that the key dimensions for the removable top enclosure (looking top down) are maintained as the length (119.5 cm) and width (76.2 cm), the height of the sides (50.8 mm), and the part's thickness (3 mm). Use the provided free CAD standard document file to replicate the removable top enclosure (squirrel) employed in this proof-of-concept study (Supplementary Coding File 2).
  2. Adjust the diameter of the through hole in the base of the platform as needed to fit the pedestal used to elevate the platform. The diameter pictured is 40 mm.
  3. Print the platform using a white opaque filament. This provides maximal contrast for the camera, enabling the tracking software to correctly detect the animal's contour on the platform.
  4. Print the removable top enclosure with opaque dark filament (e.g., red). This provides a sense of shelter for the rodents, which facilitates guiding them into the tunnel before they are lifted and transferred to the arena.
  5. Have a machinist cut the acrylic extruded clear square tube using a table saw so that the long end is ~ 101.6 mm in length. Be sure to use protective eye wear and a push stick to guide the acrylic through the blade while keeping your hands safe from potential injury.
  6. Using the table saw or a handheld rotary tool equipped with an abrasive cutting wheel, remove one of the long rectangular faces. This creates an open top through which the camera mounted above will have an unobstructed view of the animal's position and head movements.
  7. Clean all edges with a hand file or sandpaper. Assemble the modified handling tunnel using the Acrylic Extruded Clear Square Tube cut to length with the 3D printed removable top enclosure by placing the enclosure on top of the open face.

2. Setting up the OMR arena

  1. Disinfect the platform and the square tube enclosure assembly with a cleaner/disinfectant before and in between animals to remove unwanted olfactory cues.
    NOTE: While leather gloves are used to handle the animals and come into direct contact with them, they are not worn during the recordings and do not cause any lasting or observable confounding effects.
  2. Tear a small piece of paper towel measuring approximately 50 mm x 50 mm and fold it to cover the top surface of the pedestal. Place the 3D-printed platform onto the pedestal (14 inch high) with the piece of paper towel in place.
    NOTE: The paper adjusts the press fit of the platform, prevents unintended movement, provides a uniform white background for imaging (if the pedestal's surface is not white), and acts as an absorbent layer in case the animal urinates during the recording, preventing the platform from becoming slippery.
  3. Wearing leather work gloves, gently guide the animal into the square tube enclosure assembly.
  4. Transfer the animal to the arena by placing the enclosure assembly onto the platform (Figure 1J).
  5. Carefully detach the removable top enclosure leaving the animal in the acrylic extruded clear square tube on the platform. Close the door to the OMR system

3. Setting up the OMR software parameters

NOTE: The pictured OMR system uses a compact industrial camera featuring an IR-sensitive 1/3” CMOS sensor with a global shutter at 25 frames per second (fps). The camera is equipped with an F1.6 wide-angle lens, enabling a complete top-down view of the arena. Preliminary visual acuity tests conducted on squirrels using the standard 100% contrast setting revealed that the squirrels’ visual acuity exceeded the resolution limits of the hardware. The 23.8” full HD In-Plane Switching screens used in the setup have a resolution of only 1920 pixels in width, and the software is therefore hard-coded with a maximum spatial frequency of 2 cyc/°. For comparison, the visual acuity of C57Bl/6 mice is approximately 0.3-0.5 cyc/°. At 2 cyc/°, each stripe averages 5.3 pixels in width. With a rotation speed of 12°/s and a frame rate of 60 frames per second, the pattern shifts by 0.2° per frame, equivalent to 4.2 pixels per frame, assuming uniform pixel speed. At spatial frequencies near 2 cyc/°, the stripe pattern approaches the resolution limit where aliasing may occur, causing the pattern to appear as if it is moving backward. To prevent this artifact, the software is hard-coded to cap the spatial frequency at 2 cyc/°.

Thus, for squirrels we devised a protocol where we perform the acuity test but at a much lower contrast. We selected a contrast setting (12.78%) where the squirrels were unable to see the striped pattern at 2 cycles/°.

  1.  In the live video panel, ensure that the animal is adapting well to the new environment and is beginning to move less and calming down.
    1. At 2 cyc/°, each stripe averages 5.3 pixels in width. Set the rotation speed to 12°/s and a frame rate of 60 frames per second; the pattern shifts by 0.2° per frame, equivalent to 4.2 pixels per frame, assuming uniform pixel speed. Set the spatial frequencies near 2 cyc/° so the stripe pattern approaches the resolution limit where aliasing may occur, causing the pattern to appear as if it is moving backward. To prevent this artifact, hard code the software to cap the spatial frequency at 2 cyc/°.
      NOTE: For squirrels, we devised a protocol where we perform the acuity test but at a much lower contrast. We selected a contrast setting (12.78%) at which the squirrels were unable to see the striped pattern at 2 cycles/°.
  2. Download Supplementary Coding File 3. Open the OptoDrum software.
  3. Under the Settings tab, click on Import Settings. Load the Supplementary Coding File 3.
  4. Under the Settings tab, set the Background threshold offset to 17, the minimum animal size [px] to 30, and the maximum tail width [% of size] to 1.
  5. Under camera settings, leave Invert Video and Manual Camera control unchecked and IR Light Off.
  6. Widen the position and size of the region of interest for tracking to accommodate the squirrel if it leans outside of the opening of the tube. The suggested values are Position: X: 359, Y: 237, Size: X: 570, Y: 455. Do not extend the ROI over the Stimuli screen, as it can lead to false positives.
  7. Select Session Configuration from the top panel (Figure 2A).
    1. For the staircase, set estimated spatial acuity as follows. Set expected acuity to 1.800 cyc/° (648 cycles); set optimal stimulus resolution to 0.5 cyc/° (180 cycles); set measurement resolution to 0.100 cyc/° (36 cycles).
    2. For the staircase, set the number of required confirmations as follows. Set for failed trials to 3; set for successful trials to 2.
      NOTE: The number of successful trials can be increased to further reduce the occurrence of false positive confirmations. However, with the use of this platform and modified handling tunnel, the error rate remains acceptably low. This is primarily due to the squirrels' relative stillness and the infrequency of rotational head movements aside from those elicited by visually evoked stimuli.
  8. Under the Staircase tab (Figure 2B), set antialiasing to width to 3 px and leave sinusoidal unchecked.
  9. For the testing criteria, lock the Contrast at 12.78% and lock the rotation speed at 12 °/s.
    NOTE: At the 12.78% contrast setting, the squirrels' spatial acuity is limited to approximately 1.5-1.8 cyc/°. No longer exceeding the maximum hardware settings, this configuration enables the assessment of spatial acuity in response to disease or injury.
  10. Once two of the three parameters are locked, the Auto Set the parameters option will become active (no longer grayed out). Check the box next to Auto Set the Parameters.
  11. Set the rotation direction depending on whether visual impairment is expected to be in one or both eyes. Note that for each eye, only motion in the temporal-to-nasal direction elicits tracking. Consequently, assess injury to the left eye using clockwise (CW) stimulation, as counterclockwise (CCW) stimulation is expected to elicit normal responses. For degeneration or injury expected in both eyes, rotation of the stimulus in both directions may be used.
  12. Click on Start Trial to begin the presentation of the stimulus. The camera above will begin recording and tracking the animals' head movements. While the stimulus is being presented, click on the Analysis Tab for real-time viewing of the Angular Velocities (head rotation), Track Quality, and Score parameters. At the end of each stimulus presentation, the software will automatically determine whether to advance (indicated by the green checkmark) to the next Cyc/°, repeat the trial, or reduce the Cyc/° (indicated by the red X).
  13. During the recording, if the tracking software incorrectly flips the nose (red) and tail (green) markers, press Ctrl on the keyboard to allow manual override to correct the head-tail orientation.
  14. If the animal falls from the platform, pause the trial by pressing Pause Evaluation or clicking on the Space Bar. Remove the handling tunnel from the platform and use it with the lid for safe handling of the animal to place it back onto the platform. Once the animal is ready, click on Resume Evaluation to continue the trial.
  15. Once all the trials have been completed, click on the Summary Tab to show the successful trials in green and the unsuccessful trials in red. The trial circled in green indicates the visual acuity threshold for the squirrel using the contrast of 12.78%. Return the animal carefully to its home cage.

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Results

OMR is considered successful once the software identifies the visual threshold determined by the animal's performance in spatial frequency discrimination trials. Specifically, the threshold is defined as follows: two successful trials at a given spatial frequency (measured in cyc/°), followed by three failed trials at the next higher spatial frequency. OMR was performed on 13-lined ground squirrels (6-8 months of age) using the standard round flat platform (Figure 3A) to compare with the non...

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Discussion

Critical steps

Facilitating Tunnel Entry - One important point to consider is that the squirrels require the 3D-printed enclosure assembly to serve as a temporary lid for the acrylic rectangular tunnel; without it, they will not readily enter. In our facility, the 13-lined ground squirrels are regularly housed with a red rat-sized cylinder (Length: 15.24 cm, Diameter: 7.62 cm). The purpose of the 3D-printed enclosure is to provide familiarity with their enrichment tunnels, mak...

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Disclosures

Kiyoharu Miyagishima, Francisco Nadal-Nicolás, John Ball, and Wei Li declare no competing financial interests. Thomas Munch is the Owner and Director of Research and Development at Striatech GmbH. Boris Benkner is the Founder and Chief Executive Officer at Striatech GmbH.

Acknowledgements

This research was supported [in part] by the Intramural Research Program of the NIH, National Eye Institute. This work was also supported by the Office of the Assistant Secretary of Defense for Health Affairs and the Defense Health Agency J9, Research and Development Directorate, through the Vision Research Program under Award No. (CDMRPL-18-0-VR180205). Opinions, interpretations, conclusions, and recommendations are those of the author and are not necessarily endorsed by the Department of Defense. The authors thank Dr. Wenxin Ma for providing the rd10 and CX3CR1GFP/+ mice, Dr. Haohua Qian (Visual Function Core, NEI, NIH) for insightful discussion and technical assistance with the OMR, the NIMH/NINDS/NICHD machine shop for help with component fabrication, and Charles King (NIH Library) for assisting in 3D printing.

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Materials

List of materials used in this article
NameCompanyCatalog NumberComments
12V Max Lithium-ion Cordless Rotary Tool KitDremel 8220F0138220JATo cut and polish the Acrylic Square Tube.
https://www.dremel.com/us/en/p/8220-1-28-f0138220aa
6-0 COATED VICRYL (polyglactin 910) SutureEthiconJ670GFor suturing the eye lid.
https://www.ethicon.com/na/epc/code/j670g?lang=en-default
Clear Colorless Acrylic Square Tube (2" x 12")Canal Plastics CenterRT-300161Clear rectangular tunnel (for mouse).
https://www.canalplastic.com/products/clear-colorless-acrylic-square-tube
Clear Colorless Acrylic Square Tube (3" x 12")Canal Plastics CenterRT-300168Clear rectangular tunnel (for squirrel).
https://www.canalplastic.com/products/clear-colorless-acrylic-square-tube
DREMEL EZ SpeedClic: Plastic Cutting WheelsDremelSC476For cutting the Acrylic Square Tube
F270 3D printerStratasysTo print engineering grade 3D models of the platforms.
https://support.stratasys.com/en/printers/fdm-legacy/uprint
Fluriso (Isoflurane)VetOne 502017General Anesthesia. Liquid for Inhalation.
http://vetone.net/Default/GetFile?id=7dda0c60-45fa-e711-bf2e-0024e8785118
FreeCAD 1.0 Open-source parametric 3D modeler
Igor Pro software Version 6.3.7.2WaveMetrics, IncFor plotting the graphs. https://www.wavemetrics.com/
Low-Profile Anesthesia Masks for Traditional Vaporizers
 for SomnoFlo. Extra Large (animals over 300 g) 		Kent Scientific corporationSOMNO-0804For providing general anesthesia.
https://www.kentscientific.com/products/low-profile-anesthesia-masks-for-somnosuite/
MakerBot Print for Windows version 4.10.1.2056MakerBot Industries, LLCSoftware for orienting the parts for printing
MakerBot Replicator Desktop 3D Printer (5th Gen)MakerBot Industries, LLCMP05825For 3D printing prototype versions of the platforms.
https://www.rnd-tech.com/product/makerbot-replicator-desktop-3d-printer-5th-gen/
Microsoft ExcelMicrosoftSpreadsheet software to analyze the data. microsoft.com/en-us/microsoft-365/excel
Multipurpose leather work glovesSteiner IndustriesSPC02To handle squirrels.
https://www.steinerindustries.com/leather-palm/product/steiner-spc02-leather-palm-work-glove
OptoDrum PlusSTRIA.TECHCommercial device for measuring the optomotor reflex (visual acuity and contrast sensitivity) https://stria.tech/products/optodrum/ 
OptoDrum software Version 1.7.3STRIA.TECHSoftware for performing automated measures of the optomotor reflex.
Peroxigard Ready to Use (cleaner/disinfectant) PeroxigardPRTU242101To clean/disinfect the platform and the acrylid square tube between experiments.
https://peroxigard.com/product-information/rtu/
Pureline M6000 Anesthesia Machine
with O2 Concentrator		Penn Veterinary Supply, Inc.SUPM6000For animal anesthesia.
https://www.pennvet.com/customer/portal/catalog/home?urile=wcm:path%3APennVet+Catalog/Product+Catalog/SUPM6000/Pureline+M6000+Anesthesia+Mach+w_O2+Conc
uPrint SE Plus 3D printerStratasysTo print engineering grade 3D models of the platforms.
https://www.makerbot.com/makerbot-print/
White opaque MakerBot PLA Filament,
Large Spool for Replicator+ (0.9kg, 2lb)		MakerBot Industries, LLCMP05780Filament to 3D print the platforms.
https://store.ultimaker.com/3d-printer-materials/replicator-series-materials/makerbot-pla-material-large-spool-for-replicator
Pharmacological treatment
Neomycin and Polymyxin B Sulfates
and Bacitracin Zinc Ophthalmic Ointment, USP		Bausch & LombRX-0069Triple ophthalmic antibiotic for preventing ocular infections
Proparacaine Hydrochloride 0.5%Akorn17478-263-12Local anesthetic for ophthalmic instillation

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Visual AcuityContrast SensitivityNon Aversive HandlingVisual ThresholdCone Visual SystemBehavioral AssessmentHead Tracking
Non-aversive Animal Restraint Enabling Recording of Optomotor Reflex in Ground Squirrels
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