Skip to main content
Top
Published in: Documenta Ophthalmologica 3/2007

01-11-2007 | Original Reseach Article

An adaptive ERG technique to measure normal and altered dark adaptation in the mouse

Authors: Paul J. DeMarco Jr., Yoshiaki Katagiri, Volker Enzmann, Henry J. Kaplan, Maureen A. McCall

Published in: Documenta Ophthalmologica | Issue 3/2007

Login to get access

Abstract

The time-course of dark adaptation provides valuable insights into the function and interactions between the rod and cone pathways in the retina. Here we describe a technique that uses the flash electroretinogram (ERG) response to probe the functional integrity of the cone and rod pathways during the dynamic process of dark adaptation in the mouse. Retinal sensitivity was estimated from the stimulus intensity required to maintain a 30 μV criterion b-wave response during a 40 min period of dark adaptation. When tracked in this manner, dark adaptation functions in WT mice depended upon the bleaching effects of initial background adaptation conditions. Altered dark adaptation functions, commensurate with the functional deficit were recorded in pigmented mice that lacked cone function (Gnat2 cplf3 ) and in WT mice injected with a toxin, sodium iodate (NaIO3), which targets the retinal pigment epithelium and also has downstream effects on photoreceptors. These data demonstrate that this adaptive tracking procedure measures retinal sensitivity and the contributions of the rod and/or cone pathways during dark adaptation in both WT control and mutant mice.
Literature
1.
go back to reference Peachey NS, Ball SL (2003) Electrophysiological analysis of visual function in mutant mice. Doc Ophthalmol 107:13–36PubMedCrossRef Peachey NS, Ball SL (2003) Electrophysiological analysis of visual function in mutant mice. Doc Ophthalmol 107:13–36PubMedCrossRef
2.
3.
go back to reference Goto Y, Peachey NS, Ripps H, Naash MI (1995) Functional abnormalities in transgenic mice expressing a mutant rhodopsin gene. Invest Ophthalmol Vis Sci 36:62–71PubMed Goto Y, Peachey NS, Ripps H, Naash MI (1995) Functional abnormalities in transgenic mice expressing a mutant rhodopsin gene. Invest Ophthalmol Vis Sci 36:62–71PubMed
4.
go back to reference Friedburg C, Allen CP, Mason PJ, Lamb TD (2004) Contribution of cone photoreceptors and post-receptoral mechanisms to the human photopic electroretinogram. J Physiol 556:819–834PubMedCrossRef Friedburg C, Allen CP, Mason PJ, Lamb TD (2004) Contribution of cone photoreceptors and post-receptoral mechanisms to the human photopic electroretinogram. J Physiol 556:819–834PubMedCrossRef
5.
go back to reference Frishman LJ, Sieving PA (1995) Evidence for two sites of adaptation affecting the dark-adapted ERG of cats and primates. Vision Res 35:435–442PubMedCrossRef Frishman LJ, Sieving PA (1995) Evidence for two sites of adaptation affecting the dark-adapted ERG of cats and primates. Vision Res 35:435–442PubMedCrossRef
6.
go back to reference Niemeyer G (2005) ERG components of negative polarity from the inner retina and the optic nerve response. Doc Ophthalmol 111:179–189PubMedCrossRef Niemeyer G (2005) ERG components of negative polarity from the inner retina and the optic nerve response. Doc Ophthalmol 111:179–189PubMedCrossRef
7.
go back to reference Rangaswamy NV, Frishman LJ, Dorotheo EU, Schiffman JS, Bahrani HM, Tang RA (2004) Photopic ERGs in patients with optic neuropathies: comparison with primate ERGs after pharmacologic blockade of inner retina. Invest Ophthalmol Vis Sci 45:3827–3837PubMedCrossRef Rangaswamy NV, Frishman LJ, Dorotheo EU, Schiffman JS, Bahrani HM, Tang RA (2004) Photopic ERGs in patients with optic neuropathies: comparison with primate ERGs after pharmacologic blockade of inner retina. Invest Ophthalmol Vis Sci 45:3827–3837PubMedCrossRef
8.
go back to reference Saszik SM, Robson JG, Frishman LJ (2002) The scotopic threshold response of the dark-adapted electroretinogram of the mouse. J Physiol 543:899–916PubMedCrossRef Saszik SM, Robson JG, Frishman LJ (2002) The scotopic threshold response of the dark-adapted electroretinogram of the mouse. J Physiol 543:899–916PubMedCrossRef
9.
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 44:3253–3268PubMedCrossRef 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 44:3253–3268PubMedCrossRef
10.
go back to reference Chang B, Hawes NL, Hurd RE, Wang J, Howell D, Davisson MT, Roderick TH, Nusinowitz S, Heckenlively JR (2005) Mouse models of ocular diseases. Vis Neurosci 22:587–593PubMed Chang B, Hawes NL, Hurd RE, Wang J, Howell D, Davisson MT, Roderick TH, Nusinowitz S, Heckenlively JR (2005) Mouse models of ocular diseases. Vis Neurosci 22:587–593PubMed
11.
go back to reference Carter-Dawson LD, LaVail MM (1979) Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol 188:245–262PubMedCrossRef Carter-Dawson LD, LaVail MM (1979) Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol 188:245–262PubMedCrossRef
12.
go back to reference Bayer AU, Cook P, Brodie SE, Maag KP, Mittag T (2001) Evaluation of different recording parameters to establish a standard for flash electroretinography in rodents. Vision Res 41:2173–2185PubMedCrossRef Bayer AU, Cook P, Brodie SE, Maag KP, Mittag T (2001) Evaluation of different recording parameters to establish a standard for flash electroretinography in rodents. Vision Res 41:2173–2185PubMedCrossRef
13.
go back to reference Rosolen SG, Rigaudiere F, Le Gargasson JF, Brigell MG (2005) Recommendations for a toxicological screening ERG procedure in laboratory animals. Doc Ophthalmol 110:57–66PubMedCrossRef Rosolen SG, Rigaudiere F, Le Gargasson JF, Brigell MG (2005) Recommendations for a toxicological screening ERG procedure in laboratory animals. Doc Ophthalmol 110:57–66PubMedCrossRef
14.
go back to reference Peachey NS, Goto Y, al-Ubaidi MR, Naash MI (1993) Properties of the mouse cone-mediated electroretinogram during light adaptation. Neurosci Lett 162:9–11PubMedCrossRef Peachey NS, Goto Y, al-Ubaidi MR, Naash MI (1993) Properties of the mouse cone-mediated electroretinogram during light adaptation. Neurosci Lett 162:9–11PubMedCrossRef
15.
go back to reference Birch DG, Hood DC, Nusinowitz S, Pepperberg DR (1995) Abnormal activation and inactivation mechanisms of rod transduction in patients with autosomal dominant retinitis pigmentosa and the pro-23-his mutation. Invest Ophthalmol Vis Sci 36:1603–1614PubMed Birch DG, Hood DC, Nusinowitz S, Pepperberg DR (1995) Abnormal activation and inactivation mechanisms of rod transduction in patients with autosomal dominant retinitis pigmentosa and the pro-23-his mutation. Invest Ophthalmol Vis Sci 36:1603–1614PubMed
16.
go back to reference Lyubarsky AL, Pugh EN Jr. (1996) Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J Neurosci 16:563–571PubMed Lyubarsky AL, Pugh EN Jr. (1996) Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J Neurosci 16:563–571PubMed
17.
go back to reference Goto Y, Peachey NS, Ziroli NE, Seiple WH, Gryczan C, Pepperberg DR, Naash MI (1996) Rod phototransduction in transgenic mice expressing a mutant opsin gene. J Opt Soc Am A Opt Image Sci Vis 13:577–585PubMedCrossRef Goto Y, Peachey NS, Ziroli NE, Seiple WH, Gryczan C, Pepperberg DR, Naash MI (1996) Rod phototransduction in transgenic mice expressing a mutant opsin gene. J Opt Soc Am A Opt Image Sci Vis 13:577–585PubMedCrossRef
18.
go back to reference Ueda Y, Tammitsu N, Imai H, Honda Y, Shichida Y (2006) Recovery of rod-mediated a-wave during light-adaptation in mGluR6-deficient mice. Vision Res 46:1655–1664PubMedCrossRef Ueda Y, Tammitsu N, Imai H, Honda Y, Shichida Y (2006) Recovery of rod-mediated a-wave during light-adaptation in mGluR6-deficient mice. Vision Res 46:1655–1664PubMedCrossRef
19.
go back to reference Lyubarsky AL, Falsini B, Pennesi ME, Valentini P, Pugh EN Jr. (1999) UV- and midwave-sensitive cone-driven retinal responses of the mouse: a possible phenotype for coexpression of cone photopigments. J Neurosci 19:442–455PubMed Lyubarsky AL, Falsini B, Pennesi ME, Valentini P, Pugh EN Jr. (1999) UV- and midwave-sensitive cone-driven retinal responses of the mouse: a possible phenotype for coexpression of cone photopigments. J Neurosci 19:442–455PubMed
20.
go back to reference Lyubarsky AL, Chen C, Simon MI, Pugh EN Jr. (2000) Mice lacking G-protein receptor kinase 1 have profoundly slowed recovery of cone-driven retinal responses. J Neurosci 20:2209–2217PubMed Lyubarsky AL, Chen C, Simon MI, Pugh EN Jr. (2000) Mice lacking G-protein receptor kinase 1 have profoundly slowed recovery of cone-driven retinal responses. J Neurosci 20:2209–2217PubMed
21.
go back to reference Fulton AB, Manning KA, Baker BN, Schukar SE, Bailey CJ (1982) Dark-adapted sensitivity, rhodopsin content, and background adaptation in pcd/pcd mice. Invest Ophthalmol Vis Sci 22:386–393PubMed Fulton AB, Manning KA, Baker BN, Schukar SE, Bailey CJ (1982) Dark-adapted sensitivity, rhodopsin content, and background adaptation in pcd/pcd mice. Invest Ophthalmol Vis Sci 22:386–393PubMed
22.
go back to reference Perlman I (1978) Dark-adaptation in abnormal (RCS) rats studied electroretinographically. J Physiol 278:161–175PubMed Perlman I (1978) Dark-adaptation in abnormal (RCS) rats studied electroretinographically. J Physiol 278:161–175PubMed
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 26:225–239PubMedCrossRef Stockman A, Sharpe LT (2006) Into the twilight zone: the complexities of mesopic vision and luminous efficiency. Ophthalmic Physiol Opt 26:225–239PubMedCrossRef
24.
go back to reference Chang B, Dacey MS, Hawes NL, Hitchcock PF, Milam AH, Atmaca-Sonmez P, Nusinowitz S, Heckenlively JR (2006) Cone photoreceptor function loss-3, a novel mouse model of achromatopsia due to a mutation in Gnat2. Invest Ophthalmol Vis Sci 47:5017–5021PubMedCrossRef Chang B, Dacey MS, Hawes NL, Hitchcock PF, Milam AH, Atmaca-Sonmez P, Nusinowitz S, Heckenlively JR (2006) Cone photoreceptor function loss-3, a novel mouse model of achromatopsia due to a mutation in Gnat2. Invest Ophthalmol Vis Sci 47:5017–5021PubMedCrossRef
25.
go back to reference Enzmann V, Row BW, Yamauchi Y, Kheirandish L, Gozal D, Kaplan HJ, McCall MA (2006) Behavioral and anatomical abnormalities in a sodium iodate-induced model of retinal pigment epithelium degeneration. Exp Eye Res 82:441–448PubMedCrossRef Enzmann V, Row BW, Yamauchi Y, Kheirandish L, Gozal D, Kaplan HJ, McCall MA (2006) Behavioral and anatomical abnormalities in a sodium iodate-induced model of retinal pigment epithelium degeneration. Exp Eye Res 82:441–448PubMedCrossRef
26.
go back to reference Sagdullaev BT, DeMarco PJ, McCall MA (2004) Improved contact lens electrode for corneal ERG recordings in mice. Doc Ophthalmol 108:181–184PubMedCrossRef Sagdullaev BT, DeMarco PJ, McCall MA (2004) Improved contact lens electrode for corneal ERG recordings in mice. Doc Ophthalmol 108:181–184PubMedCrossRef
27.
go back to reference Lamb TD, Pugh EN Jr. (2004) Dark adaptation and the retinoid cycle of vision. Prog Retin Eye Res 23:307–380PubMedCrossRef Lamb TD, Pugh EN Jr. (2004) Dark adaptation and the retinoid cycle of vision. Prog Retin Eye Res 23:307–380PubMedCrossRef
28.
go back to reference Lyubarsky AL, Daniele LL, Pugh EN Jr. (2004) From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG. Vision Res 44:3235–3251PubMedCrossRef Lyubarsky AL, Daniele LL, Pugh EN Jr. (2004) From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG. Vision Res 44:3235–3251PubMedCrossRef
29.
go back to reference Smith SB, Hamasaki DI (1994) Electroretinographic study of the C57BL/6-mivit/mivit mouse model of retinal degeneration. Invest Ophthalmol Vis Sci 35:3119–3123PubMed Smith SB, Hamasaki DI (1994) Electroretinographic study of the C57BL/6-mivit/mivit mouse model of retinal degeneration. Invest Ophthalmol Vis Sci 35:3119–3123PubMed
30.
go back to reference Nathan J, Reh R, Ankoudinova I, Ankoudinova G, Chang B, Heckenlively J, Hurley JB (2006) Scotopic and photopic visual thresholds and spatial and temporal discrimination evaluated by behavior of mice in a water maze. Photochem Photobiol 82:1489–1494PubMedCrossRef Nathan J, Reh R, Ankoudinova I, Ankoudinova G, Chang B, Heckenlively J, Hurley JB (2006) Scotopic and photopic visual thresholds and spatial and temporal discrimination evaluated by behavior of mice in a water maze. Photochem Photobiol 82:1489–1494PubMedCrossRef
31.
go back to reference Nusinowitz S, Ridder WH 3rd, Ramirez J (2007) Temporal response properties of the primary and secondary rod-signaling pathways in normal and Gnat2 mutant mice. Exp Eye Res 84:1104–1114PubMedCrossRef Nusinowitz S, Ridder WH 3rd, Ramirez J (2007) Temporal response properties of the primary and secondary rod-signaling pathways in normal and Gnat2 mutant mice. Exp Eye Res 84:1104–1114PubMedCrossRef
32.
go back to reference Adachi-Usami E, Mizota A, Ikeda H, Hanawa T, Kimura T (1992) Transient increase of b-wave in the mouse retina after sodium iodate injection. Invest Ophthalmol Vis Sci 33:3109–3113PubMed Adachi-Usami E, Mizota A, Ikeda H, Hanawa T, Kimura T (1992) Transient increase of b-wave in the mouse retina after sodium iodate injection. Invest Ophthalmol Vis Sci 33:3109–3113PubMed
33.
go back to reference Mizota A, Adachi-Usami E (1997) Functional recovery of retina after sodium iodate injection in mice. Vision Res 37:1859–1865PubMedCrossRef Mizota A, Adachi-Usami E (1997) Functional recovery of retina after sodium iodate injection in mice. Vision Res 37:1859–1865PubMedCrossRef
34.
go back to reference Kiuchi K, Yoshizawa K, Shikata N, Moriguchi K, Tsubura A (2002) Morphologic characteristics of retinal degeneration induced by sodium iodate in mice. Curr Eye Res 25:373–379PubMedCrossRef Kiuchi K, Yoshizawa K, Shikata N, Moriguchi K, Tsubura A (2002) Morphologic characteristics of retinal degeneration induced by sodium iodate in mice. Curr Eye Res 25:373–379PubMedCrossRef
35.
go back to reference Hetling JR, Pepperberg DR (1999) Sensitivity and kinetics of mouse rod flash responses determined in vivo from paired-flash electroretinograms. J Physiol 516(Pt 2):593–609PubMedCrossRef Hetling JR, Pepperberg DR (1999) Sensitivity and kinetics of mouse rod flash responses determined in vivo from paired-flash electroretinograms. J Physiol 516(Pt 2):593–609PubMedCrossRef
36.
go back to reference Kang Derwent JJ, Qtaishat NM, Pepperberg DR (2002) Excitation and desensitization of mouse rod photoreceptors in vivo following bright adapting light. J Physiol 541:201–218PubMedCrossRef Kang Derwent JJ, Qtaishat NM, Pepperberg DR (2002) Excitation and desensitization of mouse rod photoreceptors in vivo following bright adapting light. J Physiol 541:201–218PubMedCrossRef
37.
go back to reference Cameron AM, Mahroo OA, Lamb TD (2006) Dark adaptation of human rod bipolar cells measured from the b-wave of the scotopic electroretinogram. J Physiol 575:507–526PubMedCrossRef Cameron AM, Mahroo OA, Lamb TD (2006) Dark adaptation of human rod bipolar cells measured from the b-wave of the scotopic electroretinogram. J Physiol 575:507–526PubMedCrossRef
38.
go back to reference Haig C (1941) The course of rod dark adaptation as influenced by the intensity and duration of pre-adaptation to light. J Gen Physiol 24:735–751CrossRef Haig C (1941) The course of rod dark adaptation as influenced by the intensity and duration of pre-adaptation to light. J Gen Physiol 24:735–751CrossRef
39.
go back to reference Hecht S, Haig C, Chase AM (1937) The influence of light adaptation on subsequent dark adaptation of the eye. J Gen Physiol 20:831–850CrossRef Hecht S, Haig C, Chase AM (1937) The influence of light adaptation on subsequent dark adaptation of the eye. J Gen Physiol 20:831–850CrossRef
40.
go back to reference Pugh EN (1975) Rushton’s paradox: rod dark adaptation after flash photolysis. J Physiol 248:413–431PubMed Pugh EN (1975) Rushton’s paradox: rod dark adaptation after flash photolysis. J Physiol 248:413–431PubMed
41.
go back to reference Jacobs GH, Williams GA, Fenwick JA (2004) Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse. Vision Res 44:1615–1622PubMedCrossRef Jacobs GH, Williams GA, Fenwick JA (2004) Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse. Vision Res 44:1615–1622PubMedCrossRef
42.
go back to reference Kraft TW, Schneeweis DM, Schnapf JL (1993) Visual transduction in human rod photoreceptors. J Physiol 464:747–765PubMed Kraft TW, Schneeweis DM, Schnapf JL (1993) Visual transduction in human rod photoreceptors. J Physiol 464:747–765PubMed
43.
go back to reference Schnapf JL, Kraft TW, Baylor DA (1987) Spectral sensitivity of human cone photoreceptors. Nature 325:439–441PubMedCrossRef Schnapf JL, Kraft TW, Baylor DA (1987) Spectral sensitivity of human cone photoreceptors. Nature 325:439–441PubMedCrossRef
44.
go back to reference DeMarco P, Pokorny J, Smith VC (1992) Full-spectrum cone sensitivity functions for X-chromosome-linked anomalous trichromats. J Opt Soc Am A 9:1465–1476PubMed DeMarco P, Pokorny J, Smith VC (1992) Full-spectrum cone sensitivity functions for X-chromosome-linked anomalous trichromats. J Opt Soc Am A 9:1465–1476PubMed
45.
go back to reference Norren DV, Padmos P (1974) Dark adaptation of separate cone systems studied with psychophysics and electroretinography. Vision Res 14:677–686PubMedCrossRef Norren DV, Padmos P (1974) Dark adaptation of separate cone systems studied with psychophysics and electroretinography. Vision Res 14:677–686PubMedCrossRef
Metadata
Title
An adaptive ERG technique to measure normal and altered dark adaptation in the mouse
Authors
Paul J. DeMarco Jr.
Yoshiaki Katagiri
Volker Enzmann
Henry J. Kaplan
Maureen A. McCall
Publication date
01-11-2007
Publisher
Springer-Verlag
Published in
Documenta Ophthalmologica / Issue 3/2007
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-007-9078-5

Other articles of this Issue 3/2007

Documenta Ophthalmologica 3/2007 Go to the issue