Predation without direction selectivity

Author:

Krizan Jenna12,Song Xiayingfang13,Fitzpatrick Michael J.12ORCID,Shen Ning1ORCID,Soto Florentina1ORCID,Kerschensteiner Daniel145ORCID

Affiliation:

1. Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, MO 63110

2. Graduate program in Neuroscience, Roy and Diana Vagelos Division of Biology and Biomedical Sciences, Washington University School of Medicine, St. Louis, MO 63110

3. Graduate program in Biomedical Engineering, Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO 63130

4. Department of Neuroscience, Washington University School of Medicine, St. Louis, MO 63110

5. Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO 63130

Abstract

Across the animal kingdom, visual predation relies on motion-sensing neurons in the superior colliculus (SC) and its orthologs. These neurons exhibit complex stimulus preferences, including direction selectivity, which is thought to be critical for tracking the unpredictable escape routes of prey. The source of direction selectivity in the SC is contested, and its contributions to predation have not been tested experimentally. Here, we use type-specific cell removal to show that narrow-field (NF) neurons in the mouse SC guide predation. In vivo recordings demonstrate that direction-selective responses of NF cells are independent of recently reported stimulus-edge effects. Monosynaptic retrograde tracing reveals that NF cells receive synaptic input from direction-selective ganglion cells. When we eliminate direction selectivity in the retina of adult mice, direction-selective responses in the SC, including in NF cells, are lost. However, eliminating retinal direction selectivity does not affect the hunting success or strategies of mice, even when direction selectivity is removed after mice have learned to hunt, and despite abolishing the gaze-stabilizing optokinetic reflex. Thus, our results identify the retinal source of direction selectivity in the SC. They show that NF cells in the SC guide predation, an essential spatial orienting task, independent of their direction selectivity, revealing behavioral multiplexing of complex neural feature preferences and highlighting the importance of feature-selective manipulations for neuroethology.

Funder

HHS | NIH | National Eye Institute

Publisher

Proceedings of the National Academy of Sciences

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