A new role for photoresponsive neurons called simple photoreceptors in the sea slug Onchidium verruculatum: Potentiation of synaptic transmission and motor response

The simple photoreceptors Ip-1 and Ip-2 are intrinsically light-sensitive neurons that exist in the abdominal ganglion of the sea slug Onchidium verruculatum. Using isolated ganglia and semi-intact or intact animal preparations, the present studies examined the light-sensing and physiological roles of Ip-1 and Ip-2 cells, which respond jointly to light by inducing a slow hyperpolarizing receptor potential. First, the synaptic inputs received by Ip-1 and Ip-2 and the axonal branches arising from their cell bodies were investigated. We found that these cells are not only first-order photosensory neurons, but also second-order neurons (interneurons), relaying inhibitory synaptic inputs such as water pressure and/or tactile senses. The amphibian Onchidium opens a pneumostome at low tide in order to aero-breathe. This pneumostome opening; i.e., aero-breathing behavior, was produced by spike discharges of Ip-1 and Ip-2 cells. Furthermore, the present results suggested that the hyperpolarizing photoresponse of Ip-1 and Ip-2 cells operates in the potentiation of inhibitory sensory synaptic transmission. Thus, we conclude that the simple photoreceptors of Onchidium play a role in the long-lasting potentiation of synaptic transmission and the subsequent behavioral response and so may be involved in a new photosensory modality, non-image-forming vision.