Detection sensitivity and temporal resolution of visual signals near absolute threshold in the salamander retina

Several studies have suggested that the visual system can detect dim lights with a fidelity limited only by Poisson fluctuations in photon absorption and spontaneous activation of rhodopsin. If correct, this implies that neural processing of responses produced by rod photoreceptors is efficient and effectively noiseless. However, experimental uncertainty makes this conclusion tenuous. Furthermore, previous work provided no information about how accurately stimulus timing is represented. Here, the detection sensitivity and temporal resolution of salamander rods and retinal ganglion cells (RGCs) are compared in nearly matched experimental conditions by using recorded responses to identify the time of a flash. At detection threshold, RGCs could reliably signal the absorption of 20-50 photons, but the rods within the RGC receptive field could signal stimuli 3-10 times weaker. For flash strengths 10 times higher than detection threshold, some RGCs could distinguish stimulus timing with a resolution finer than 100 msec, within a factor of 2 of the rod limit. The relationship between RGC and rod sensitivity could not be explained by added noise in the retinal circuitry but could be explained by a threshold acting after pooling of rod signals. Simulations of rod signals indicated that continuous noise, rather than spontaneous activation of rhodopsin or fluctuations in the single-photon response, limited temporal resolution. Thus, detection of dim lights was limited by retinal processing, but, at higher light levels, synaptic transmission, cellular integration of synaptic inputs, and spike generation in RGCs faithfully conveyed information about the time of photon absorption.