An offset ON–OFF receptive field is created by gap junctions between distinct types of retinal ganglion cells

In the vertebrate retina, the location of a neuron’s receptive field in visual space closely corresponds to the physical location of synaptic input onto its dendrites, a relationship called the retinotopic map. We report the discovery of a systematic spatial offset between the ON and OFF receptive subfields in F-mini-ON retinal ganglion cells (RGCs). Surprisingly, this property does not come from spatially offset ON and OFF layer dendrites, but instead arises from a network of electrical synapses via gap junctions to RGCs of a different type, the F-mini-OFF. We show that the asymmetric morphology and connectivity of these RGCs can explain their receptive field offset, and we use a multicell model to explore the effects of receptive field offset on the precision of edge-location representation in a population. This RGC network forms a new electrical channel combining the ON and OFF feedforward pathways within the output layer of the retina.