Abstract
Animals investigate their environments by directing their gaze towards salient stimuli. In the prevailing view, mouse gaze shifts entail head rotations followed by brainstem-mediated eye movements, including saccades to reset the eyes. These 'recentering' saccades are attributed to head movement-related vestibular cues. However, microstimulating mouse superior colliculus (SC) elicits directed head and eye movements resembling SC-dependent sensory-guided gaze shifts in other species, suggesting that mouse gaze shifts may be more flexible than has been recognized. 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 directionally biased saccades coincident with attempted head rotations. Differences in saccade endpoints across stimuli are associated with distinct stimulus-dependent relationships between initial eye position and saccade direction and amplitude. Optogenetic perturbations revealed SC drives these gaze shifts. Thus, head-fixed mice make sensory-guided, SC-dependent gaze shifts involving coincident, directionally biased saccades and attempted head movements. Our findings uncover flexibility in mouse gaze shifts and provide a foundation for studying head-eye coupling.
Highlights
Natural environments are complex and dynamic, and animals frequently redirect their gaze to scrutinize salient sensory stimuli
Mice are an increasingly important model organism in 37 vision research, yet the strategies they use to shift their gaze remain incompletely understood. Revealing these strategies is essential to understanding mouse visual ethology and the underlying neural mechanisms. 41 The prevailing view holds that species whose retinae lack high-acuity specializations such as mice generate gaze shifts driven by head movements and followed by “recentering” saccades (Land and Nilsson, 2012)
Consistent with our prediction, ear airpuff-evoked saccades were typically not preceded by slow attempted head rotations but were accompanied by roughly coincident fast attempted head rotations (Figure 4B, D, F). On average, these fast attempted head rotations had similar peak velocities and latencies relative to saccade onset to those observed from SC optogenetic stimulation as well as those made during the fast phase of head movements during spontaneous gaze shifts (Figure 4B, D). This pattern was mirrored in the average eye and attempted head movement traces for whisker airpuff, auditory airpuff, and ear tactile-evoked saccades (Figure 4—figure supplement 1A-D). 261 To better understand how these patterns arose, we examined eye and attempted head 262 movement timing at the single-trial level
Summary
Animals investigate their environments by directing their gaze towards salient stimuli. Mouse gaze shifts entail head rotations followed by brainstem-mediated eye movements, including saccades to reset the eyes. These “recentering” saccades are attributed to head movement-related vestibular cues. Microstimulating mouse superior colliculus (SC) elicits directed head and eye movements resembling SC-dependent sensory-guided gaze shifts in other species, suggesting that mouse gaze shifts may be more flexible than has been recognized. We investigated this possibility by tracking eye and attempted head movements in a head-fixed preparation that eliminates head movement-related sensory cues. Our findings uncover flexibility in mouse gaze shifts and provide a foundation for studying head-eye coupling
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