Non-preferred contrast responses in the Drosophila motion pathways reveal a receptive field structure that explains a common visual illusion

• Published in: Current biology 2021-12, Vol.31 (23), p.5286-5298.e7
• Main Authors: Gruntman, Eyal, Reimers, Pablo, Romani, Sandro, Reiser, Michael B.
• Format: Article
• Language: English
• Subjects: Animals; directional selectivity; Drosophila; Drosophila - physiology; Illusions; Motion Perception - physiology; motion vision; Neurons - physiology; ON/OFF pathways; reverse-phi illusion; T4/T5; Visual Pathways - physiology
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.09.072

Diverse sensory systems, from audition to thermosensation, feature a separation of inputs into ON (increments) and OFF (decrements) signals. In the Drosophila visual system, separate ON and OFF pathways compute the direction of motion, yet anatomical and functional studies have identified some crosstalk between these channels. We used this well-studied circuit to ask whether the motion computation depends on ON-OFF pathway crosstalk. Using whole-cell electrophysiology, we recorded visual responses of T4 (ON) and T5 (OFF) cells, mapped their composite ON-OFF receptive fields, and found that they share a similar spatiotemporal structure. We fit a biophysical model to these receptive fields that accurately predicts directionally selective T4 and T5 responses to both ON and OFF moving stimuli. This model also provides a detailed mechanistic explanation for the directional preference inversion in response to the prominent reverse-phi illusion. Finally, we used the steering responses of tethered flying flies to validate the model’s predicted effects of varying stimulus parameters on the behavioral turning inversion. •Whole-cell recordings of T4 and T5 responses to ON-OFF visual stimuli•T4 and T5 have a similar receptive field but with opposite contrast selectivity•Biophysical model fit to ON and OFF responses predicts directional selectivity•The model explains cellular and behavioral responses to reverse-phi illusion Recording whole-cell responses from ON and OFF cells in the Drosophila motion pathway, Gruntman et al. show that these cells share a receptive field structure for their non-preferred contrast responses. This structure explains the perception of directional inversion to the reverse-phi illusion.