Physiological characterization of a rare subpopulation of doublet-spiking neurons in the ferret lateral geniculate nucleus

Interest in exploring homologies in the early visual pathways of rodents, carnivores, and primates has recently grown. Retinas of these species contain morphologically and physiologically heterogeneous retinal ganglion cells that form the basis for parallel visual information processing streams. Whether rare retinal ganglion cells with unusual visual response properties in carnivores and primates project to the visual thalamus and drive unusual visual responses among thalamic relay neurons is poorly understood. We surveyed neurophysiological responses among hundreds of lateral geniculate nucleus (LGN) neurons in ferrets and observed a novel subpopulation of LGN neurons displaying doublet-spiking waveforms. Some visual response properties of doublet-spiking LGN neurons, like contrast and temporal frequency tuning, were intermediate to those of X and Y LGN neurons. Interestingly, most doublet-spiking LGN neurons were tuned for orientation and displayed direction selectivity for horizontal motion. Spatiotemporal receptive fields of doublet-spiking neurons were diverse and included center/surround organization, On/Off responses, and elongated separate On and Off subregions. Optogenetic activation of corticogeniculate feedback did not alter the tuning or spatiotemporal receptive fields of doublet-spiking neurons, suggesting that their unusual tuning properties were inherited from retinal inputs. The doublet-spiking LGN neurons were found throughout the depth of LGN recording penetrations. Together these findings suggest that while extremely rare (<2% of recorded LGN neurons), unique subpopulations of LGN neurons in carnivores receive retinal inputs that confer them with nonstandard visual response properties like direction selectivity. These results suggest that neuronal circuits for nonstandard visual computations are common across a variety of species, even though their proportions vary. NEW & NOTEWORTHY Interest in visual system homologies across species has recently increased. Across species, retinas contain diverse retinal ganglion cells including cells with unusual visual response properties. It is unclear whether rare retinal ganglion cells in carnivores project to and drive similarly unique visual responses in the visual thalamus. We discovered a rare subpopulation of thalamic neurons defined by unique spike shape and visual response properties, suggesting that nonstandard visual computations are common to many species.