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Nonlinearity and noise at the rod—rod bipolar cell synapse

  • E. BRADY TREXLER (a1) (a2), ALEXANDER R.R. CASTI (a3) (a2) and YU ZHANG (a4)

In the retina, rod bipolar (RBP) cells synapse with many rods, and suppression of rod outer segment and synaptic noise is necessary for their detection of rod single-photon responses (SPRs). Depending on the rods’ signal-to-noise ratio (SNR), the suppression mechanism will likely eliminate some SPRs as well, resulting in decreased quantum efficiency. We examined this synapse in rabbit, where 100 rods converge onto each RBP. Suction electrode recordings showed that rabbit rod SPRs were difficult to distinguish from noise (independent SNR estimates were 2.3 and 2.8). Nonlinear transmission from rods to RBPs improved response detection (SNR = 8.7), but a large portion of the rod SPRs was discarded. For the dimmest flashes, the loss approached 90%. Despite the high rejection ratio, noise of two distinct types was apparent in the RBP traces: low-amplitude rumblings and discrete events that resembled the SPR. The SPR-like event frequency suggests that they result from thermal isomerizations of rhodopsin, which occurred at the rate 0.033/s/rod. The presence of low-amplitude noise is explained by a sigmoidal input–output relationship at the rod—RBP synapse and the input of noisy rods. The rabbit rod SNR and RBP quantum efficiency are the lowest yet reported, suggesting that the quantum efficiency of the rod—RBP synapse may depend on the SNR in rods. These results point to the possibility that fewer photoisomerizations are discarded for species such as primate, which has a higher rod SNR.

Corresponding author
*Address correspondence and reprint requests to: E. Brady Trexler, Department of Ophthalmology, Mount Sinai School of Medicine, 1 Gustave L. Levy Place, Box 1183, New York, NY 10029. E-mail:
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Barlow, H.B. (1957). Increment thresholds at low intensities considered as signal/noise discriminations. The Journal of Physiology 136, 469488.
Baylor, D.A., Lamb, T.D. & Yau, K.W. (1979 a). Responses of retinal rods to single photons. The Journal of Physiology 288, 613634.
Baylor, D.A., Lamb, T.D. & Yau, K.W. (1979 b). The membrane current of single rod outer segments. The Journal of Physiology 288, 589611.
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. The Journal of Physiology 357, 575607.
Berntson, A., Smith, R.G. & Taylor, W.R. (2004). Transmission of single photon signals through a binary synapse in the mammalian retina. Visual Neuroscience 21, 693702.
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal and Eye Research 20, 351384.
Burns, M.E., Mendez, A., Chen, J. & Baylor, D.A. (2002). Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36, 8191.
Campbell, N.R. (1909). The study of discontinuous phenomena. Proceedings of the Cambridge Philosophical Society 15, 117136.
Clark, P.T. & van Rossum, M.C. (2006). The optimal synapse for sparse, binary signals in the rod pathway. Neural Computation 18, 2644.
Dhingra, A., Faurobert, E., Dascal, N., Sterling, P. & Vardi, N. (2004). A retinal-specific regulator of G-protein signaling interacts with Galpha(o) and accelerates an expressed metabotropic glutamate receptor 6 cascade. The Journal of Neuroscience 24, 56845693.
Dhingra, A., Jiang, M., Wang, T.L., Lyubarsky, A., Savchenko, A., Bar-Yehuda, T., Sterling, P., Birnbaumer, L. & Vardi, N. (2002). Light response of retinal ON bipolar cells requires a specific splice variant of Galpha(o). The Journal of Neuroscience 22, 48784884.
Dhingra, A., Lyubarsky, A., Jiang, M., Pugh, E.N., Birnbaumer, L., Sterling, P. & Vardi, N. (2000). The light response of ON bipolar neurons requires G[alpha]o. The Journal of Neuroscience 20, 90539058.
Dodge, F.A., Knight, B.W. & Toyoda, J. (1968). Voltage noise in limulus visual cells. Science 160, 8890.
Fain, G.L., Matthews, H.R. & Cornwall, M.C. (1996). Dark adaptation in vertebrate photoreceptors. Trends in Neurosciences 19, 502507.
Field, G.D. & Rieke, F. (2002). Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34, 773785.
Field, G.D., Sampath, A.P. & Rieke, F. (2005). Retinal processing near absolute threshold: From behavior to mechanism. Annual Review of Physiology 67, 491514.
Grunert, U., Martin, P.R. & Wassle, H. (1994). Immunocytochemical analysis of bipolar cells in the macaque monkey retina. The Journal of Comparative Neurology 348, 607627.
Hecht, S., Shlaer, S. & Pirenne, M.H. (1942). Energy, quanta, and vision. The Journal of General Physiology 25, 819840.
Hornstein, E.P., Verweij, J., Li, P.H. & Schnapf, J.L. (2005). Gap-junctional coupling and absolute sensitivity of photoreceptors in macaque retina. The Jounal of Neuroscience 25, 1120111209.
Lamb, T.D. (1995). Photoreceptor spectral sensitivities: Common shape in the long-wavelength region. Vision Research 35, 30833091.
Lane, J.A. (1984). The central limit theorem for the Poisson shot-noise process. Journal of Applied Probability 21, 287301.
Li, W., Keung, J.W. & Massey, S.C. (2004). Direct synaptic connections between rods and OFF cone bipolar cells in the rabbit retina. The Journal of Comparative Neurology 474, 112.
Morgans, C.W., Brown, R.L. & Duvoisin, R.M. (2010). TRPM1: The endpoint of the mGluR6 signal transduction cascade in retinal ON-bipolar cells. BioEssays 32, 609614.
Nakatani, K., Tamura, T. & Yau, K.W. (1991). Light adaptation in retinal rods of the rabbit and two other nonprimate mammals. The Journal of General Physiology 97, 413435.
Pan, F. & Massey, S.C. (2007). Rod and cone input to horizontal cells in the rabbit retina. The Journal of Comparative Neurology 500, 815831.
Rao, R., Buchsbaum, G. & Sterling, P. (1994). Rate of quantal transmitter release at the mammalian rod synapse. Biophysical Journal 67, 5763.
Rieke, F. & Baylor, D.A. (1996). Molecular origin of continuous dark noise in rod photoreceptors. Biophysical Journal 71, 25532572.
Robson, J.G., Maeda, H., Saszik, S.M. & Frishman, L.J. (2004). In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vision Research 44, 32533268.
Sakitt, B. (1972). Counting every quantum. The Journal of Physiology 223, 131150.
Sampath, A.P. & Rieke, F. (2004). Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41, 431443.
Schneeweis, D.M. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 10531056.
Schneeweis, D.M. & Schnapf, J.L. (2000). Noise and light adaptation in rods of the macaque monkey. Visual Neuroscience 17, 659666.
Shen, Y., Heimel, J.A., Kamermans, M., Peachey, N.S., Gregg, R.G. & Nawy, S. (2009). A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. The Journal of Neuroscience 29, 60886093.
Sterling, P. & Smith, R.G. (2004). Design for a binary synapse. Neuron 41, 313315.
Taylor, W.R. & Smith, R.G. (2004). Transmission of scotopic signals from the rod to rod-bipolar cell in the mammalian retina. Vision Research 44, 32693276.
Trexler, E.B., Li, W. & Massey, S.C. (2005). Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses. Journal of Neurophysiology 93, 14761485.
Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. (2001). Microcircuits for night vision in mouse retina. The Journal of Neuroscience 21, 86168623.
van Rossum, M.C. & Smith, R.G. (1998). Noise removal at the rod synapse of mammalian retina. Visual Neuroscience 15, 809821.
Wilson, M. (2002). Retinal processing: Smaller babies thrown out with bathwater. Current Biology 12, R625R627.
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Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
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