Saccadic surpression: from zebrafish to primates

Aristides Arrenberg – Universität Tübingen
Ziad Hafed – Universität Tübingen

Active sensing is the mode of operation for most behaving organisms. While there are a multitude of computational advantages to active sensing, moving the sensor, such as the eyes, invariably introduces complexities in the processing of input sensory streams. Here, we study the robust phenomenon that visual processing is strongly altered around the time of rapid saccades. During “saccadic suppression”, detection thresholds for brief visual stimulus presentations are dramatically elevated, and during “saccadic remapping”, receptive fields briefly change despite their principal retinotopy. Although saccadic suppression and remapping are robust phenomena, countless debates have emerged, and remain, about their mechanisms and origins. Our goal in the proposed research is to approach saccadic suppression and remapping from the perspective of evolutionary convergence and optimization, and we will do so by studying two organisms at two opposite ends of the evolutionary spectrum: zebrafish and non-human primates. We focus on the optic tectum (OT) in fish and the homologous superior colliculus (SC) in monkeys. In the first funding period, we demonstrated saccadic suppression in zebrafish for the first time, and we linked its properties to novel results in the monkey superior colliculus (SC). Saccadic suppression is apparently weaker and longer-lasting in fish than in monkeys. To understand potential convergent evolutionary principles that might explain both the qualitative similarities and quantitative differences between species, we built a computational control theory model invoking efficient sensorimotor estimation as the mechanism for suppression. In this framework, the SC/OT shares computational resources for both motor control and visual perception, and parameters like sensory and motor noise may account for quantitative differences between distinct animal lineages. In the second funding period, we will leverage our success in the experimental collection part of the first funding period to provide well-grounded biological constraints that will improve the explanatory power of the model. Importantly, we will also expand our experimental approach to reveal the properties of spatial receptive field remapping in the two species. Our results will demonstrate a functional-level convergence of the SC/OT and showcase the performance limits of vision. Our approach is decidedly unique: the same personnel will directly work with both species, in a close collaboration across two neighboring laboratories, allowing the deepest insights possible. This approach was particularly fruitful in the first funding period, and we will further capitalize on it in the current project. The transformative aspect of our proposal is that we will study active vision in zebrafish, and that we will use the experimental accessibility in the fish OT and its evolutionarily more ancient brain to clarify long-lasting debates about the involvement of mammalian SC in similar phenomena.