Ganglion cell performance at absolute threshold in toad retina: effects of dark events in rods.

1. The performance of ganglion cells in detecting flashes of light near the absolute threshold was studied in an isolated eye‐cup preparation of toad retina. Retinal ganglion cells, through which all visual information from the rods must flow to the brain, are in a key position for evaluating the still unproven hypothesis that the absolute light sensitivity is limited by rod noise (Barlow, 1956). 2. The dark‐adapted threshold intensity for these cells, which were selected on the basis of their high sensitivity, averaged 0.029 Rh* flash‐1 (range 0.008‐0.062), where Rh* signifies one photoisomerization per rod. On average, 46 photoisomerizations were needed per receptive field per flash to evoke a threshold response (range 16‐84). 3. In the threshold region, frequency of responses versus mean flash intensity was determined. Threshold performance could be described by theoretical frequency of response curves, allowing intrinsic noise to be estimated in terms of an equivalent rate of photoisomerization‐like (dark) events. In two completely characterized cells the rate of dark events corresponded to 0.03 and 0.06 Rh*DS‐1, where Rh*D signifies one dark event per rod. 4. Threshold elevations produced by dim backgrounds were studied. The results of these experiments are consistent with a dark event rate equivalent to 0.046 Rh*DS‐1, or 0.037 Rh*DS‐1 after correcting for a probable decrease in summation time. 5. The rate of actual dark events (0.028 Rh*DS‐1, 20 degrees C) measured in Bufo rods (Baylor, Lamb & Yau, 1980) is close to the equivalent rates determined here. Thus, for the ganglion cells signalling the dimmest lights, the dark events in rods appear to be the most significant intrinsic retinal noise source limiting detection.

[1]  G. Fain,et al.  Sensitivity of toad rods: Dependence on wave‐length and background illumination. , 1976, The Journal of physiology.

[2]  B. Cleland,et al.  Quantitative aspects of sensitivity and summation in the cat retina , 1968, The Journal of physiology.

[3]  A. Rose,et al.  The Relative Sensitivities of Television Pickup Tubes, Photographic Film, and the Human Eye , 1942, Proceedings of the IRE.

[4]  D. Copenhagen,et al.  Does the random distribution of discrete photoreceptor events limit the sensitivity of the retina? , 1986, Neuroscience Research.

[5]  S. Hecht,et al.  ENERGY, QUANTA, AND VISION , 1942, The Journal of general physiology.

[6]  W. Stell,et al.  Rod and cone inputs to bipolar cells in goldfish retina , 1980, The Journal of comparative neurology.

[7]  A. Rose The sensitivity performance of the human eye on an absolute scale. , 1948, Journal of the Optical Society of America.

[8]  A. Hodgkin,et al.  Detection and resolution of visual stimuli by turtle photoreceptors , 1973, The Journal of physiology.

[9]  H. Barlow Retinal noise and absolute threshold. , 1956, Journal of the Optical Society of America.

[10]  G. Matthews Dark noise in the outer segment membrane current of green rod photoreceptors from toad retina. , 1984, The Journal of physiology.

[11]  K. Donner,et al.  The dark-adaptation of single units in the frog's retina and its relation to the regeneration of rhodopsin. , 1965, Vision research.

[12]  Richard H. White,et al.  Rhodopsin and Porphyropsin Fields In the Adult Bullfrog Retina , 1971, The Journal of general physiology.

[13]  G Falk,et al.  An analysis of voltage noise in rod bipolar cells of the dogfish retina. , 1982, The Journal of physiology.

[14]  C. Bridges,et al.  Molar Absorbance Coefficient of Rhodopsin , 1970, Nature.

[15]  W. G. Owen,et al.  Functional characteristics of lateral interactions between rods in the retina of the snapping turtle. , 1976, The Journal of physiology.

[16]  P. Lillywhite,et al.  Multiplicative intrinsic noise and the limits to visual performance , 1981, Vision Research.

[17]  M W Levine,et al.  Statistics of the maintained discharge of cat retinal ganglion cells. , 1983, The Journal of physiology.

[18]  C. Baumann,et al.  The dark adaptation of single units in the isolated frog retina following partial bleaching of rhodopsin. , 1968, Vision research.

[19]  H. Dartnall The photosensitivities of visual pigments in the presence of hydroxylamine. , 1968, Vision research.

[20]  D. Baylor,et al.  Two components of electrical dark noise in toad retinal rod outer segments. , 1980, The Journal of physiology.

[21]  G. Fain,et al.  Quantum sensitivity of rods in the toad retina. , 1975, Science.

[22]  H. Barlow Chapter 16 – THE PHYSICAL LIMITS OF VISUAL DISCRIMINATION , 1964 .

[23]  H. Barlow,et al.  Responses to single quanta of light in retinal ganglion cells of the cat. , 1971, Vision research.

[24]  G. H. Gold Photoreceptor coupling in retina of the toad, Bufo marinus. II. Physiology. , 1979, Journal of neurophysiology.

[25]  K. Brown,et al.  Effects of Ba2+upon the dark-adapted intensity-response curve of toad rods , 1979, Vision Research.

[26]  T. Reuter,et al.  Receptive field organization of ganglion cells in the frog retina: contributions from cones, green rods and red rods. , 1975, The Journal of physiology.

[27]  H. Barlow Summation and inhibition in the frog's retina , 1953, The Journal of physiology.

[28]  S Hemilä,et al.  Directional selectivity and colour coding in the frog retina. , 1978, Medical biology.

[29]  D. Baylor,et al.  The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. , 1984, The Journal of physiology.

[30]  G. Fain,et al.  Light adaptation in toad rods: requirement for an internal messenger which is not calcium. , 1979, The Journal of physiology.

[31]  W. Stiles,et al.  Saturation of the Rod Mechanism of the Retina at High Levels of Stimulation , 1954 .

[32]  J. Ashmore,et al.  Dark noise in retinal bipolar cells and stability of rhodopsin in rods , 1977, Nature.

[33]  K. Donner Adaptation-related changes in the spatial and temporal summation of frog retinal ganglion cells. , 1987, Acta physiologica Scandinavica.

[34]  L. Pinto,et al.  Interactions among rods in the isolated retina of Bufo marinus. , 1981, The Journal of physiology.

[35]  D. Copenhagen,et al.  Evidence for passive electrotonic interactions in red rods of toad retina , 1978, Nature.

[36]  H B BARLOW,et al.  Increment thresholds at low intensities considered as signal/noise discriminations , 1957, The Journal of physiology.

[37]  H. Vries The quantum character of light and its bearing upon threshold of vision, the differential sensitivity and visual acuity of the eye , 1943 .