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A new type of mouse gaze shift is led by directed saccades

Citation

Zahler, Sebastian et al. (2021), A new type of mouse gaze shift is led by directed saccades, Dryad, Dataset, https://doi.org/10.7272/Q6V69GTV

Abstract

Animals investigate their environments by directing their gaze towards salient stimuli. In the prevailing view, mouse gaze shifts are led by head rotations that trigger compensatory, brainstem-mediated eye movements, including saccades to reset the eyes. These “recentering” saccades are attributed to head movement-related vestibular and optokinetic cues. However, microstimulating mouse superior colliculus (SC) elicits directed head and eye movements that resemble SC-dependent sensory-guided gaze shifts made by other species, raising the possibility mice generate additional types of gaze shifts. We investigated this possibility by tracking eye and attempted head movements in a head-fixed preparation that eliminates head movement-related sensory cues. We found tactile stimuli evoke gaze shifts involving directed saccades that precede attempted head rotations. Optogenetic perturbations revealed SC drives touch-evoked gaze shifts. Thus, mice make sensory-guided, SC-dependent gaze shifts led by directed saccades. Our findings uncover diversity in mouse gaze shifts and provide a foundation for studying head-eye coupling.

Methods

In these experiments, a camera recorded the left pupils of awake head-fixed mice while left or right stimuli were randomly presented in 7-12 s intervals. Each session (360 stimulus presentations) used one of four stimulation protocols: 1) whisker airpuff, 2) ear airpuff, 3) auditory-only airpuff, and 4) tactile-only whisker bar.

Airpuff stimuli were generated using 3D-printed nozzles connected to compressed air gated by a solenoid. For whisker airpuffs, the nozzles were positioned beneath the mouse’s left and right whiskers. For ear airpuffs, the nozzles were directed at the ears. For auditory-only airpuffs, the nozzles were moved away from the mouse to avoid deflecting whiskers while maintaining the same azimuthal position. For tactile-only whisker stimulation, the whiskers were deflected along an axis parallel to whisking motion using an L-key attached to a stepper motor.

Unless otherwise noted, pupil video data was collected at 50 Hz. DeepLabCut was used to extract the left and right edges of both the pupil and the corneal reflection of an IR LED. Angular eye position (E) was determined using the formula: E = arcsin((CR-P)/Rp), where CR is the position of the corneal reflection center, P is the position of the pupil center, and Rp (1.08 mm) is the estimated radius of rotation of the pupil. Saccades were defined as eye movements that exceeded 100°/s, were at least 2° in amplitude, and were not preceded by a saccade in the previous 100 ms. The initial positions and endpoints of saccades were defined as the first points at which saccade velocity rose above or fell below 50°/s, respectively. In the subset of experiments that examined the relationship between saccade amplitude and velocity and bilateral eye movements, both eyes were recorded at 200 Hz.  In an additional subset of experiments, attempted head movements were measured using load cells (a.k.a., strain gauges).

In a subset of experiments, optogenetic manipulations of SC were performed in conjunction with the whisker airpuff stimulation. Optogenetic illumination was delivered on a random 50% of trials using 1 s of illumination centered around airpuff onset. For optogenetic inactivation of SC neurons, AAV1.hSyn.eNpHR3.0 was injected in right SC. For subthreshold optogenetic stimulation of SC neurons, AAV1.CaMKIIa.hChR2(H134R)-EYFP was injected in right SC. To control for the effects of light and viral expression, AAV9.CaMKII.GCaMP6s was injected in SC of 4 wild-type mice.

Usage Notes

DeepLabCut reports prediction confidence using likelihood values. Rather than analyze faulty data points, frames containing any points with DeepLabCut-calculated likelihood of P < 0.99 have been set to NaNs.

Sessions from the same mouse under the same stimulation protocol have been combined into single time series. 

For our paper, mice were excluded from analysis for a given stimulus type (e.g., whisker airpuff) if the probability of a saccade during the response window (within 150 ms of stimulus) across all sessions was below 5%. We have not excluded mice or sessions from this dataset.

Funding

National Institute of Mental Health, Award: DP2 MH119426

National Institute of Neurological Disorders and Stroke, Award: R01 NS109060

Simons Foundation Autism Research Initiative, Award: 574347

Klingenstein-Simons Fellowship Award in Neuroscience

Whitehall Foundation

E. Matilda Ziegler Foundation for the Blind

Brain and Behavior Research Foundation, Award: 25337

Brain and Behavior Research Foundation, Award: 27320

Sandler Foundation