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Published in: Documenta Ophthalmologica 3/2011

01-12-2011 | Original Research Article

An extended 15 Hz ERG protocol (1): the contributions of primary and secondary rod pathways and the cone pathway

Authors: Mieke M. C. Bijveld, Astrid M. L. Kappers, Frans C. C. Riemslag, Frank P. Hoeben, Anne C. L. Vrijling, Maria M. van Genderen

Published in: Documenta Ophthalmologica | Issue 3/2011

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Abstract

The minimum in the amplitude versus flash strength curve of dark-adapted 15 Hz electroretinograms (ERGs) has been attributed to interactions between the primary and secondary rod pathways. The 15 Hz ERGs can be used to examine the two rod pathways in patients. However, previous studies suggested that the cone-driven pathway also contributes to the 15 Hz ERGs for flash strengths just above that of the minimum. We investigated cone pathway contributions to improve upon the interpretation of (abnormal) 15 Hz ERGs measured in patients. We recorded 15 Hz ERGs in five healthy volunteers, using a range of flash strengths that we extended to high values. The stimuli were varied in both colour (blue, green, amber, and red) and flash duration (short flash and square wave) in order to stimulate rods and cones in various ways. The differences in the responses to the four colours could be fully explained by the spectral sensitivity of rods for flash strengths up to approximately 12.5 log quanta·deg−2. At higher flash strengths, higher-order harmonics appeared in the responses which could be attributed to cones being more sensitive than rods to higher frequencies. Furthermore, the amplitude curves of the blue and green responses showed a second minimum suggesting rod to cone interactions. We present a descriptive model of the contributions of the rod and cone pathways. In clinical application, we would advise using the short flash flicker instead of the square wave flicker, as the responses are of larger amplitude, and cone pathway contributions can be recognized from large higher-order harmonics.
Footnotes
1
For the analysis of linear and non-linear response components, the sine-wave is the best choice but this was not optional in our experimental set-up. However, as described in previous studies, responses to square wave flicker are similar to sine wave responses [11, 28, 38].
 
Literature
1.
go back to reference Bloomfield SA, Dacheux RF (2001) Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20(3):351–384PubMedCrossRef Bloomfield SA, Dacheux RF (2001) Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20(3):351–384PubMedCrossRef
2.
go back to reference Volgyi B, Deans MR, Paul DL, Bloomfield SA (2004) Convergence and segregation of the multiple rod pathways in mammalian retina. J Neurosci 24(49):11182–11192PubMedCrossRef Volgyi B, Deans MR, Paul DL, Bloomfield SA (2004) Convergence and segregation of the multiple rod pathways in mammalian retina. J Neurosci 24(49):11182–11192PubMedCrossRef
3.
4.
go back to reference Robson JG, Maeda H, Saszik SM, Frishman LJ (2004) In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vision Res 44(28):3253–3268PubMedCrossRef Robson JG, Maeda H, Saszik SM, Frishman LJ (2004) In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vision Res 44(28):3253–3268PubMedCrossRef
5.
go back to reference Sampath AP, Rieke F (2004) Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41(3):431–443PubMedCrossRef Sampath AP, Rieke F (2004) Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41(3):431–443PubMedCrossRef
6.
go back to reference Dunn FA, Doan T, Sampath AP, Rieke F (2006) Controlling the gain of rod-mediated signals in the mammalian retina. J Neurosci 26(15):3959–3970PubMedCrossRef Dunn FA, Doan T, Sampath AP, Rieke F (2006) Controlling the gain of rod-mediated signals in the mammalian retina. J Neurosci 26(15):3959–3970PubMedCrossRef
7.
go back to reference Sharpe LT, Stockman A (1999) Rod pathways: the importance of seeing nothing. Trends Neurosci 22(11):497–504PubMedCrossRef Sharpe LT, Stockman A (1999) Rod pathways: the importance of seeing nothing. Trends Neurosci 22(11):497–504PubMedCrossRef
8.
9.
go back to reference Conner JD (1982) The temporal properties of rod vision. J Physiol 332:139–155PubMed Conner JD (1982) The temporal properties of rod vision. J Physiol 332:139–155PubMed
10.
go back to reference Sharpe LT, Stockman A, MacLeod DI (1989) Rod flicker perception: scotopic duality, phase lags and destructive interference. Vision Res 29(11):1539–1559PubMedCrossRef Sharpe LT, Stockman A, MacLeod DI (1989) Rod flicker perception: scotopic duality, phase lags and destructive interference. Vision Res 29(11):1539–1559PubMedCrossRef
11.
go back to reference Sharpe LT, Fach CC, Stockman A (1993) The spectral properties of the two rod pathways. Vision Res 33(18):2705–2720PubMedCrossRef Sharpe LT, Fach CC, Stockman A (1993) The spectral properties of the two rod pathways. Vision Res 33(18):2705–2720PubMedCrossRef
12.
go back to reference Sharpe LT, Hofmeister J, Fach CC, Stockman A (1994) Spatial relations of flicker signals in the two rod pathways in man. J Physiol 474(3):421–431PubMed Sharpe LT, Hofmeister J, Fach CC, Stockman A (1994) Spatial relations of flicker signals in the two rod pathways in man. J Physiol 474(3):421–431PubMed
13.
go back to reference Stockman A, Sharpe LT, Zrenner E, Nordby K (1991) Slow and fast pathways in the human rod visual system: electrophysiology and psychophysics. J Opt Soc Am A 8(10):1657–1665PubMedCrossRef Stockman A, Sharpe LT, Zrenner E, Nordby K (1991) Slow and fast pathways in the human rod visual system: electrophysiology and psychophysics. J Opt Soc Am A 8(10):1657–1665PubMedCrossRef
14.
go back to reference Stockman A, Sharpe LT, Ruther K, Nordby K (1995) Two signals in the human rod visual system: a model based on electrophysiological data. Vis Neurosci 12(5):951–970PubMedCrossRef Stockman A, Sharpe LT, Ruther K, Nordby K (1995) Two signals in the human rod visual system: a model based on electrophysiological data. Vis Neurosci 12(5):951–970PubMedCrossRef
15.
go back to reference Scholl HP, Langrova H, Weber BH, Zrenner E, Apfelstedt-Sylla E (2001) Clinical electrophysiology of two rod pathways: Normative values and clinical application. Graefes Arch Clin Exp Ophthalmol 239(2):71–80PubMedCrossRef Scholl HP, Langrova H, Weber BH, Zrenner E, Apfelstedt-Sylla E (2001) Clinical electrophysiology of two rod pathways: Normative values and clinical application. Graefes Arch Clin Exp Ophthalmol 239(2):71–80PubMedCrossRef
16.
go back to reference Scholl HP, Langrova H, Pusch CM, Wissinger B, Zrenner E, Apfelstedt-Sylla E (2001) Slow and fast rod ERG pathways in patients with X-linked complete stationary night blindness carrying mutations in the NYX gene. Invest Ophthalmol Vis Sci 42(11):2728–2736PubMed Scholl HP, Langrova H, Pusch CM, Wissinger B, Zrenner E, Apfelstedt-Sylla E (2001) Slow and fast rod ERG pathways in patients with X-linked complete stationary night blindness carrying mutations in the NYX gene. Invest Ophthalmol Vis Sci 42(11):2728–2736PubMed
17.
go back to reference Scholl HP, Besch D, Vonthein R, Weber BH, Apfelstedt-Sylla E (2002) Alterations of slow and fast rod ERG signals in patients with molecularly confirmed stargardt disease type 1. Invest Ophthalmol Vis Sci 43(4):1248–1256PubMed Scholl HP, Besch D, Vonthein R, Weber BH, Apfelstedt-Sylla E (2002) Alterations of slow and fast rod ERG signals in patients with molecularly confirmed stargardt disease type 1. Invest Ophthalmol Vis Sci 43(4):1248–1256PubMed
18.
go back to reference Zeitz C, van Genderen M, Neidhardt J, Luhmann UF, Hoeben F, Forster U, Wycisk K, Matyas G, Hoyng CB, Riemslag F, Meire F, Cremers FP, Berger W (2005) Mutations in GRM6 cause autosomal recessive congenital stationary night blindness with a distinctive scotopic 15-Hz flicker electroretinogram. Invest Ophthalmol Vis Sci 46(11):4328–4335PubMedCrossRef Zeitz C, van Genderen M, Neidhardt J, Luhmann UF, Hoeben F, Forster U, Wycisk K, Matyas G, Hoyng CB, Riemslag F, Meire F, Cremers FP, Berger W (2005) Mutations in GRM6 cause autosomal recessive congenital stationary night blindness with a distinctive scotopic 15-Hz flicker electroretinogram. Invest Ophthalmol Vis Sci 46(11):4328–4335PubMedCrossRef
19.
go back to reference Littink KW, van Genderen MM, Collin RW, Roosing S, de Brouwer AP, Riemslag FC, Venselaar H, Thiadens AA, Hoyng CB, Rohrschneider K, den Hollander AI, Cremers FP, van den Born LI (2009) A novel homozygous nonsense mutation in CABP4 causes congenital cone-rod synaptic disorder. Invest Ophthalmol Vis Sci 50(5):2344–2350PubMedCrossRef Littink KW, van Genderen MM, Collin RW, Roosing S, de Brouwer AP, Riemslag FC, Venselaar H, Thiadens AA, Hoyng CB, Rohrschneider K, den Hollander AI, Cremers FP, van den Born LI (2009) A novel homozygous nonsense mutation in CABP4 causes congenital cone-rod synaptic disorder. Invest Ophthalmol Vis Sci 50(5):2344–2350PubMedCrossRef
20.
go back to reference van Genderen MM, Bijveld MM, Claassen YB, Florijn RJ, Pearring JN, Meire FM, McCall MA, Riemslag FC, Gregg RG, Bergen AA, Kamermans M (2009) Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. Am J Hum Genet 85(5):730–736PubMedCrossRef van Genderen MM, Bijveld MM, Claassen YB, Florijn RJ, Pearring JN, Meire FM, McCall MA, Riemslag FC, Gregg RG, Bergen AA, Kamermans M (2009) Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. Am J Hum Genet 85(5):730–736PubMedCrossRef
21.
go back to reference Ruther K, Sharpe LT, Zrenner E (1994) Dual rod pathways in complete achromatopsia. Ger J Ophthalmol 3(6):433–439PubMed Ruther K, Sharpe LT, Zrenner E (1994) Dual rod pathways in complete achromatopsia. Ger J Ophthalmol 3(6):433–439PubMed
22.
go back to reference CIE (1926) Commission internationale de l’Eclairage proceedings CIE (1926) Commission internationale de l’Eclairage proceedings
23.
go back to reference Stockman A, Sharpe LT (2006) Into the twilight zone: the complexities of mesopic vision and luminous efficiency. Ophthalmic Physiol Opt 26(3):225–239PubMedCrossRef Stockman A, Sharpe LT (2006) Into the twilight zone: the complexities of mesopic vision and luminous efficiency. Ophthalmic Physiol Opt 26(3):225–239PubMedCrossRef
24.
go back to reference Padmos P, van Norren D (1971) Cone spectral sensitivity and chromatic adaptation as revealed by human flicker-electroretinography. Vision Res 11(1):27–42PubMedCrossRef Padmos P, van Norren D (1971) Cone spectral sensitivity and chromatic adaptation as revealed by human flicker-electroretinography. Vision Res 11(1):27–42PubMedCrossRef
25.
go back to reference Burns SA, Elsner AE, Kreitz MR (1992) Analysis of nonlinearities in the flicker ERG. Optom Vis Sci 69(2):95–105PubMedCrossRef Burns SA, Elsner AE, Kreitz MR (1992) Analysis of nonlinearities in the flicker ERG. Optom Vis Sci 69(2):95–105PubMedCrossRef
26.
go back to reference Odom JV, Reits D, Burgers N, Riemslag FC (1992) Flicker electroretinograms: a systems analytic approach. Optom Vis Sci 69(2):106–116PubMedCrossRef Odom JV, Reits D, Burgers N, Riemslag FC (1992) Flicker electroretinograms: a systems analytic approach. Optom Vis Sci 69(2):106–116PubMedCrossRef
27.
go back to reference Verma R, Pianta MJ (2009) The contribution of human cone photoreceptors to the photopic flicker electroretinogram. J Vis 9(3):9.1–12 Verma R, Pianta MJ (2009) The contribution of human cone photoreceptors to the photopic flicker electroretinogram. J Vis 9(3):9.1–12
28.
go back to reference Kondo M, Sieving PA (2002) Post-photoreceptoral activity dominates primate photopic 32-Hz ERG for sine-, square-, and pulsed stimuli. Invest Ophthalmol Vis Sci 43(7):2500–2507PubMed Kondo M, Sieving PA (2002) Post-photoreceptoral activity dominates primate photopic 32-Hz ERG for sine-, square-, and pulsed stimuli. Invest Ophthalmol Vis Sci 43(7):2500–2507PubMed
29.
go back to reference McCulloch DL, Hamilton R (2010) Essentials of photometry for clinical electrophysiology of vision. Doc Ophthalmol 121(1):77–84PubMedCrossRef McCulloch DL, Hamilton R (2010) Essentials of photometry for clinical electrophysiology of vision. Doc Ophthalmol 121(1):77–84PubMedCrossRef
30.
31.
go back to reference Marmor MF, Fishman GA (1989) At last. A standard electroretinography protocol. Arch Ophthalmol 107(6):813–814PubMedCrossRef Marmor MF, Fishman GA (1989) At last. A standard electroretinography protocol. Arch Ophthalmol 107(6):813–814PubMedCrossRef
32.
go back to reference Dawson WW, Trick GL, Litzkow CA (1979) Improved electrode for electroretinography. Invest Ophthalmol Vis Sci 18(9):988–991PubMed Dawson WW, Trick GL, Litzkow CA (1979) Improved electrode for electroretinography. Invest Ophthalmol Vis Sci 18(9):988–991PubMed
33.
go back to reference Meigen T, Bach M (1999) On the statistical significance of electrophysiological steady-state responses. Doc Ophthalmol 98(3):207–232PubMedCrossRef Meigen T, Bach M (1999) On the statistical significance of electrophysiological steady-state responses. Doc Ophthalmol 98(3):207–232PubMedCrossRef
34.
go back to reference Nusinowitz S, Ridder WH III, Ramirez J (2007) Temporal response properties of the primary and secondary rod-signaling pathways in normal and Gnat2 mutant mice. Exp Eye Res 84(6):1104–1114PubMedCrossRef Nusinowitz S, Ridder WH III, Ramirez J (2007) Temporal response properties of the primary and secondary rod-signaling pathways in normal and Gnat2 mutant mice. Exp Eye Res 84(6):1104–1114PubMedCrossRef
35.
go back to reference Gouras P, Gunkel RD (1964) The frequency response of normal, rod achromat and nyctalope ERGs to sinusoidal monochromatic light stimulation. Doc Ophthalmol 18(1):137–150PubMedCrossRef Gouras P, Gunkel RD (1964) The frequency response of normal, rod achromat and nyctalope ERGs to sinusoidal monochromatic light stimulation. Doc Ophthalmol 18(1):137–150PubMedCrossRef
36.
go back to reference Arden GB, Carter RM, Hogg CR (1983) A modified ERG technique and the results obtained in X-linked retinitis pigmentosa. Br J Ophthalmol 67(7):419–430PubMedCrossRef Arden GB, Carter RM, Hogg CR (1983) A modified ERG technique and the results obtained in X-linked retinitis pigmentosa. Br J Ophthalmol 67(7):419–430PubMedCrossRef
37.
go back to reference Carpenter RHS, Robson JG (1999) Vision research: a practical guide to laboratory methods. Oxford University Press, Oxford Carpenter RHS, Robson JG (1999) Vision research: a practical guide to laboratory methods. Oxford University Press, Oxford
38.
go back to reference Bush RA, Sieving PA (1996) Inner retinal contributions to the primate photopic fast flicker electroretinogram. J Opt Soc Am A Opt Image Sci Vis 13(3):557–565PubMedCrossRef Bush RA, Sieving PA (1996) Inner retinal contributions to the primate photopic fast flicker electroretinogram. J Opt Soc Am A Opt Image Sci Vis 13(3):557–565PubMedCrossRef
Metadata
Title
An extended 15 Hz ERG protocol (1): the contributions of primary and secondary rod pathways and the cone pathway
Authors
Mieke M. C. Bijveld
Astrid M. L. Kappers
Frans C. C. Riemslag
Frank P. Hoeben
Anne C. L. Vrijling
Maria M. van Genderen
Publication date
01-12-2011
Publisher
Springer-Verlag
Published in
Documenta Ophthalmologica / Issue 3/2011
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-011-9292-z

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