Taking it slow: A positive feedback chloride current in cone photoreceptors supports slow motion detection

Abstract

Photoreceptors gate and shape visual information. Since perception ultimately guides action, the way photoreceptors transform light into neural signals constrains an animals behavioural repertoire. Yet, the physiological role of the highly conserved calcium-dependent chloride current in cone photoreceptors has remained elusive. Whereas calcium-activated currents typically provide negative feedback, we identify a counter-intuitive positive feedback mechanism that enhances detection of slow motion. Using genetics, electrophysiology, and behavioural assays in zebrafish, we show that loss of this current exaggerates the biphasic character of cone impulse responses and diminishes their voltage response amplitude to low temporal frequencies (<1 Hz). These changes in photoreceptor properties translate to behaviour, reducing the gain of the optokinetic response to slow-moving stimuli. Mechanistically, the calcium-dependent chloride current acts as a positive feedback loop that sustains the photovoltage response and counteracts strong adaptation within the cone phototransduction cascade. This functional role is conserved across sensory modalities, as demonstrated by similar temporal integration and amplification observed in the odorant system.