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

Abstract

Receptive fields (RFs) are a foundational concept in sensory neuroscience. The RF of a sensory neuron is shaped by the properties of its synaptic inputs from connected neurons. In the early visual system, retinotopic maps define a strict relationship between the location of a cell's dendrites and its RF location in visual space 1-3 . Retinal ganglion cells (RGCs), the output cells of the retina, form dendritic mosaics that tile retinal space and have corresponding RF mosaics that tile visual space 1,2 . The precise location of dendrites in some RGCs has been shown to predict their RF shape 4 . Previously described ON-OFF RGCs have aligned dendrites in ON and OFF synaptic layers, so the cells respond to increments and decrements of light at the same locations in visual space [5][6][7][8] . Here we report a systematic offset between the ON and OFF RFs of an RGC type. Surprisingly, this property does not come from offset ON and OFF dendrites but instead arises from electrical synapses with RGCs of a different type. This circuit represents a new channel for direct communication between ON and OFF RGCs. Using a multi-cell model, we find that offset ON-OFF RFs could improve the precision with which edge location is represented in an RGC population.1

Feedback from retinal ganglion cells to the inner retina

“…First, we found both positive and negative couplings between ganglion cells of the same response polarities (Fig 3A Consistently, such a cross-talk between the ON and OFF channels via gap junctions has been reported recently [34]. Taken together, negative couplings are suggested to be formed exclusively between ganglion cells of the same response polarities.…”

Feedback from retinal ganglion cells to the inner retina

“…In contrast, positive couplings dominated between the cell pairs with different response polarities ( Figure 3C,D,H and Supplementary Figure 3C,D,H for salamander cells; mouse data not analyzed because the coupled model performance did not improve significantly; Figure 2D and Supplementary Figure 1E). Consistently, such a cross-talk between the ON and OFF channels via gap junctions has been reported recently (Cooler and Schwartz, 2021). Taken together, negative couplings are suggested to be formed exclusively between ganglion cells of the same response polarities.…”

“…We next analyzed the model parameters to gain insights into the retinal circuits underlying ganglion cell couplings and to derive experimentally testable predictions. The data sets from ON and OFF cells were combined here as they showed the same trend (Fig 3 Consistently, such a cross-talk between the ON and OFF channels via gap junctions has been reported recently [34]. Taken together, negative couplings are suggested to be formed exclusively between ganglion cells of the same response polarities.…”

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

“…Additionally, our models are only trained to reproduce the static receptive field of T4 and T5 neurons, but are used to predict responses to dynamic stimuli such as moving bars, edges, and minimal reverse-phi motion. Our model is also the first (to our knowledge) in flies to incorporate stimulus offset responses (see [47] in mice). These offset components provide an intuitive explanation for why moving NC bars cause directionally selective responses while moving edges with the same contrast do not (Fig 4A), and they play a critical role in generating the inverted directional preference to reverse-phi motion (Fig.…”