Saccadic Suppression Enhances Saliency of Prey-Like Stimuli in the Optic Tectum

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Abstract

Saccadic suppression, a reduction in visual sensitivity around the time of rapid eye movements, is well-documented in primate psychophysics but its mechanisms and functions remain debated. Here, we use zebrafish to trace the origins of saccadic suppression and we demonstrate how saccadic suppression selectively enhances the visual salience of ecologically relevant stimuli. Saccadic suppression thus contributes to more than just compensation for rapid saccade-induced image shifts. We first established a behavioral correlate of saccadic suppression in larval zebrafish escape behavior. Then, using electrophysiology, we show that retinal ganglion cells jumpstart saccadic suppression in a spatial frequency dependent manner. Calcium imaging, combined with 360° visual stimulation and behavioral tracking, revealed that motor signals enhance peri-saccadic suppression strength in the optic tectum, where suppression lasts for more than 3000 ms. Notably, saccadic suppression is much weaker and more short-lived for stimuli related to hunting or escape behavior than for behaviorally less relevant global flashes. This unequal attenuation effectively increases the salience of the ecologically relevant stimuli in the optic tectum after saccades. Our results demonstrate that saccadic suppression integrates visual and motor signals to optimize sensory processing within neural constraints, and they provide insights into evolutionarily conserved visual strategies.
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Abstract Saccadic suppression, a reduction in visual sensitivity around the time of rapid eye movements, is well-documented in primate psychophysics but its mechanisms and functions remain debated. Here, we use zebrafish to trace the origins of saccadic suppression and we demonstrate how saccadic suppression selectively enhances the visual salience of ecologically relevant stimuli. Saccadic suppression thus contributes to more than just compensation for rapid saccade-induced image shifts. We first established a behavioral correlate of saccadic suppression in larval zebrafish escape behavior. Then, using electrophysiology, we show that retinal ganglion cells jumpstart saccadic suppression in a spatial frequency dependent manner. Calcium imaging, combined with 360° visual stimulation and behavioral tracking, revealed that motor signals enhance peri-saccadic suppression strength in the optic tectum, where suppression lasts for more than 3000 ms. Notably, saccadic suppression is much weaker and more short-lived for stimuli related to hunting or escape behavior than for behaviorally less relevant global flashes. This unequal attenuation effectively increases the salience of the ecologically relevant stimuli in the optic tectum after saccades. Our results demonstrate that saccadic suppression integrates visual and motor signals to optimize sensory processing within neural constraints, and they provide insights into evolutionarily conserved visual strategies. Competing Interest Statement The authors have declared no competing interest. Footnotes Additional author was added. Figure 1 and 4 were added after additional experiments were conducted. Text was updated accordingly. Revisions for clarity to existing figures and text. Comprehensive update of supplementary materials. Data availability The scripts and the required pre-processed dataset for the figures and supplementary figures included in the current study are available in a public repository (https://doi.gin.g-node.org/…) upon publication. The retinal electrophysiology data and raw calcium imaging data supporting the current study have not been deposited in a public repository because of their large size but are available from the corresponding author on request.

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License: CC-BY-NC-ND-4.0