Physiological basis of resolution acuity in vision

Vision is the primary sensory modality for many animals, especially humans and other primates. A fundamental constraint on visual resolution acuity is set by the size and spacing of cone photoreceptors, notably in the fovea of the retina where cones are the smallest. To optimally utilise this cone array, neurons in the retina and lateral geniculate nucleus (LGN) must have receptive field centres comprised of only one cone, yet such receptive fields have never been observed directly. Here we comprehensively map parafoveal LGN receptive fields in male macaques using an adaptive optics microstimulator and align them to the underlying cone mosaic. The receptive field centres of parvocellular LGN neurons were most often defined by signals originating from a single cone photoreceptor, a finding confirmed by biophysical light capture modelling and spatial frequency tuning data. Our results demonstrate that visual acuity originating at the fovea is mediated by LGN neurons working at the limit of cone photoreceptor spacing. Revealing this physiological basis of spatial resolution reconciles longstanding anatomical and perceptual data over what mechanism limits acuity prior to cortical processing, underscoring the centrality of optical correction for attaining peak visual resolving power. Neural mechanisms underlying high visual acuity are not fully understood. Here the authors show that high resolution visual information is transmitted from the retina to the brain by neurons in the parvocellular geniculate pathway in macaques, where signals are now shown to most often originate from single cone photoreceptors, establishing the neural mechanism that limits resolution acuity prior to cortical processing.