Classic experiments (Hecht et al. 1942; van der Velden, 1944) show that dark-adapted humans can detect dim flashes producing only a handful of photons. Yet we still do not fully understand the neural mechanisms that allow this striking sensitivity, nor do we understand where in the visual pathway the absolute limit of vision is set. We investigated these questions for the first time in the outputs of primate retina by recording the responses of ON-parasol ganglion cells (magnocellular-projecting neurons) using patch clamp technique. Surprisingly, ON-parasols nonlinearly integrated signals originating from single photon absorptions in retinal inputs in complete darkness. Integration became linear in the presence of dim background light. The release of nonlinearity was associated with a significant drop in the signal-to-noise ratio of ON-parasols. The neural location underlying this novel nonlinearity has access to several hundreds rod photoreceptors, and cannot be explained by any known nonlinearity in the retinal circuitry. These results, together with an earlier finding of a thresholding nonlinearity upstream in the same mammalian retinal circuit (Field & Rieke, 2002), are consistent with the idea that nonlinearities operating at different levels of convergence of sparse input signals protect them from being buried under neural noise. This general strategy of nonlinear signal transmission and noise filtering at multiple levels of convergence in a multiunit neural circuit has implications far beyond the visual system. In vision, this novel nonlinearity operates at the absolute threshold and sets a fundamental limit to detection.