Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-23T16:41:22.531Z Has data issue: false hasContentIssue false
  • English
  • Français

Nonlinearity and noise at the rod—rod bipolar cell synapse

Published online by Cambridge University Press:  04 November 2010

E. BRADY TREXLER ,
ALEXANDER R.R. CASTI  and
YU ZHANG
E. BRADY TREXLER*
Affiliation:
Department of Ophthalmology, Mount Sinai, New York, New York Department of Neuroscience, Mount Sinai, New York, New York
ALEXANDER R.R. CASTI
Affiliation:
Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, New Jersey Department of Neuroscience, Mount Sinai, New York, New York
YU ZHANG
Affiliation:
Department of Pharmacology and Systems Therapeutics, Mount Sinai, New York, New York
*
*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: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

Retinal bipolar cellThermal isomerizationQuantum efficiencyPhotoreceptorConvergence
Type
Research Article
Information
Visual Neuroscience , Volume 28 , Issue 1 , January 2011 , pp. 61 - 68
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barlow, H.B. (1957). Increment thresholds at low intensities considered as signal/noise discriminations. The Journal of Physiology 136, 469–488.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.W. (1979 a). Responses of retinal rods to single photons. The Journal of Physiology 288, 613–634.Google Scholar
Baylor, D.A., Lamb, T.D. & Yau, K.W. (1979 b). The membrane current of single rod outer segments. The Journal of Physiology 288, 589–611.Google Scholar
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, 575–607.CrossRefGoogle ScholarPubMed
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, 693–702.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal and Eye Research 20, 351–384.Google Scholar
Burns, M.E., Mendez, A., Chen, J. & Baylor, D.A. (2002). Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36, 81–91.Google Scholar
Campbell, N.R. (1909). The study of discontinuous phenomena. Proceedings of the Cambridge Philosophical Society 15, 117–136.Google Scholar
Clark, P.T. & van Rossum, M.C. (2006). The optimal synapse for sparse, binary signals in the rod pathway. Neural Computation 18, 26–44.Google Scholar
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, 5684–5693.Google Scholar
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, 4878–4884.CrossRefGoogle ScholarPubMed
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, 9053–9058.Google Scholar
Dodge, F.A., Knight, B.W. & Toyoda, J. (1968). Voltage noise in limulus visual cells. Science 160, 88–90.Google Scholar
Fain, G.L., Matthews, H.R. & Cornwall, M.C. (1996). Dark adaptation in vertebrate photoreceptors. Trends in Neurosciences 19, 502–507.Google Scholar
Field, G.D. & Rieke, F. (2002). Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34, 773–785.Google Scholar
Field, G.D., Sampath, A.P. & Rieke, F. (2005). Retinal processing near absolute threshold: From behavior to mechanism. Annual Review of Physiology 67, 491–514.Google Scholar
Grunert, U., Martin, P.R. & Wassle, H. (1994). Immunocytochemical analysis of bipolar cells in the macaque monkey retina. The Journal of Comparative Neurology 348, 607–627.Google Scholar
Hecht, S., Shlaer, S. & Pirenne, M.H. (1942). Energy, quanta, and vision. The Journal of General Physiology 25, 819–840.Google Scholar
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, 11201–11209.CrossRefGoogle ScholarPubMed
Lamb, T.D. (1995). Photoreceptor spectral sensitivities: Common shape in the long-wavelength region. Vision Research 35, 3083–3091.Google Scholar
Lane, J.A. (1984). The central limit theorem for the Poisson shot-noise process. Journal of Applied Probability 21, 287–301.Google Scholar
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, 1–12.Google Scholar
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, 609–614.CrossRefGoogle ScholarPubMed
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, 413–435.CrossRefGoogle ScholarPubMed
Pan, F. & Massey, S.C. (2007). Rod and cone input to horizontal cells in the rabbit retina. The Journal of Comparative Neurology 500, 815–831.Google Scholar
Rao, R., Buchsbaum, G. & Sterling, P. (1994). Rate of quantal transmitter release at the mammalian rod synapse. Biophysical Journal 67, 57–63.CrossRefGoogle ScholarPubMed
Rieke, F. & Baylor, D.A. (1996). Molecular origin of continuous dark noise in rod photoreceptors. Biophysical Journal 71, 2553–2572.Google Scholar
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, 3253–3268.CrossRefGoogle ScholarPubMed
Sakitt, B. (1972). Counting every quantum. The Journal of Physiology 223, 131–150.Google Scholar
Sampath, A.P. & Rieke, F. (2004). Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41, 431–443.CrossRefGoogle ScholarPubMed
Schneeweis, D.M. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.CrossRefGoogle ScholarPubMed
Schneeweis, D.M. & Schnapf, J.L. (2000). Noise and light adaptation in rods of the macaque monkey. Visual Neuroscience 17, 659–666.CrossRefGoogle ScholarPubMed
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, 6088–6093.CrossRefGoogle ScholarPubMed
Sterling, P. & Smith, R.G. (2004). Design for a binary synapse. Neuron 41, 313–315.CrossRefGoogle ScholarPubMed
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, 3269–3276.Google Scholar
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, 1476–1485.Google Scholar
Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. (2001). Microcircuits for night vision in mouse retina. The Journal of Neuroscience 21, 8616–8623.Google Scholar
van Rossum, M.C. & Smith, R.G. (1998). Noise removal at the rod synapse of mammalian retina. Visual Neuroscience 15, 809–821.CrossRefGoogle ScholarPubMed
Wilson, M. (2002). Retinal processing: Smaller babies thrown out with bathwater. Current Biology 12, R625–R627.Google Scholar