Electrophysiology and transcriptomics reveal two photoreceptor classes and complex visual integration in Hirudo verbana
Among animals with complex visual processing mechanisms, the leech Hirudo verbana is a rare example in which all neurons can be identified. However, little is known about its visual system, which is composed of several pigmented head eyes and photosensitive non-pigmented sensilla that are distributed across its entire body. Although several interneurons are known to respond to visual stimuli, their response properties are poorly understood. Among these, the S cell system is especially intriguing: It is multimodal, spans the entire body of the leech, and is thought to be involved in complex sensory integration. To improve our understanding of the role of this system, we tested its spectral sensitivity, spatial integration, and adaptation properties. The response of the S cell system to visual stimuli was found to be strongly dependent on the size of the area stimulated, and adaptation was local. Furthermore, a "bleaching experiment" demonstrated that at least two color channels contributed to the response, and that their contribution was dependent on the adaptation to the background. The existence of at least two color channels was further supported by transcriptomic evidence, which indicated the existence of at least two distinct groups of putative opsins for leeches. Taken together, our results show that the S cell system has highly sophisticated response properties, and could be involved in the processing of complex visual stimuli. We propose the leech as a novel system to understand visual processing mechanisms with many practical advantages. Summary statementDetailed quantitative analysis of light responses in the medicinal leech Hirudo verbana unequivocally demonstrates the existence of parallel visual pathways processing visual and UV stimuli. Responses to spatially complex stimuli indicate relatively sophisticated information processing.