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Dark Light, Rod Saturation, and the Absolute and Incremental Sensitivity of Mouse Cone Vision

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Dark Light, Rod Saturation, and the Absolute and Incremental Sensitivity of Mouse Cone Vision The Journal of Neuroscience, September 15, 2010 • 30(37):12495–12507 • 12495 Behavioral/Systems/Cognitive Dark Light, Rod Saturation, and the Absolute and Incremental Sensitivity of Mouse Cone Vision Frank Naarendorp,1 Tricia M. Esdaille,1 Serenity M. Banden,1 John Andrews-Labenski,2 Owen P. Gross,3 and Edward N. Pugh Jr3 1Department of Psychology, Northeastern University, Boston, Massachusetts 02115, 2Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, and 3Center for Neuroscience, University of California, Davis, Davis, California 95616 Visual thresholds of mice for the detection of small, brief targets were measured with a novel behavioral methodology in the dark and in the ϳ presenceofadaptinglightsspanning 8log10 unitsofintensity.Tohelpdissectthecontributionsofrodandconepathways,bothwild-typemice and mice lacking rod (Gnat1 Ϫ/Ϫ) or cone (Gnat2cpfl3) function were studied. Overall, the visual sensitivity of mice was found to be remarkably similartothatofthehumanperipheralretina.Rodabsolutethresholdcorrespondedto12–15isomerizedpigmentmolecules(R*)inimagefields of 800 to 3000 rods. Rod “dark light” (intrinsic retinal noise in darkness) corresponded to that estimated previously from single-cell recordings, 0.012R*sϪ1rod Ϫ1,indicatingthatspontaneousthermalisomerizationsareresponsible.Psychophysicalrodsaturationwasmeasuredforthefirsttime inanonhumanspeciesandfoundtobeverysimilartothatofthehumanrodmonochromat.Conethresholdcorrespondedtoϳ5R*cone Ϫ1inanimage fieldof280cones.Conedarklightwasequivalenttoϳ5000R*sϪ1cone Ϫ1,consistentwithprimatesingle-celldatabut100-foldhigherthanpredictedby recentmeasurementsoftherateofthermalisomerizationofmouseconeopsins,indicatingthatnonopsinsourcesofnoisedetermineconethreshold.The new, fully automated behavioral method is based on the ability of mice to learn to interrupt spontaneous wheel running on the presentation of a visual cue and provides an efficient and highly reliable means of examining visual function in naturally behaving normal and mutant mice. Introduction threshold sensitivity (Barlow, 1956, 1972). It is widely held that the The study of human visual sensitivity was greatly advanced in the neural mechanisms underlying the sensitivity and adaptive proper- 20th century with the development of precision psychophysics ties of the visual system revealed in human increment threshold devoted to the measurement of thresholds for small, brief stimuli investigations reside in the retina, though definitive evidence for this delivered to prescribed retinal locations and presented to the claim has not yet been provided. An adequate animal model in dark-adapted eye or in the presence of an adapting background which to investigate these classic features of the visual system would or “conditioning field.” One classical example of such work is provide a means for determining their neural mechanisms. that of Hecht et al. (1941), which unequivocally established that The mouse is now the species most widely used for the exper- rods in the dark-adapted human retina could signal the capture imental investigation of nervous system function and the molec- of individual photons. Also classic are the investigations of Stiles ular mechanisms of its diseases. Reasons for this choice include (Stiles, 1939, 1949; Aguilar and Stiles, 1954; Stiles, 1959) with the the genomic proximity of mice to humans, the great array of “two-color increment threshold” method, which uses monochro- molecular tools for making targeted gene manipulations in mice, matic adapting backgrounds and test stimuli of different and varied the vast knowledge base of molecular, cellular and behavioral wavelengths. These investigations revealed component branches of experimentation using mice, the large number of mouse lines threshold versus intensity (t.v.i.) curves governing light adaptation, that already exist with targeted manipulations in genes of rele- and quantified many novel and important features of the threshold vance to visual function and disease, the relatively short genera- sensitivity and light adaptation of the visual system. Such features tion time, and the economics of mouse husbandry. Though include the absolute and relative sensitivities of rod and cone path- extensively used in the investigation of basic retinal function and ways and estimation of the “dark light” of the signaling pathways of genetic eye disease, the value of the mouse for eye research would each photoreceptor class. Dark light refers to intrinsic visual system be enhanced considerably were it possible to measure visual sen- noise present in complete darkness that acts as a determinant of sitivity quantitatively and noninvasively in the manner of Stiles (1939). Here, we attempt to achieve this goal. Received April 27, 2010; revised June 24, 2010; accepted July 19, 2010. Materials and Methods This work was supported by National Institutes of Health Grant EY-02660 to E.N.P. and funds from the Research Mouse husbandry and strain sources to Prevent Blindness Foundation. We are grateful to Drs. Marie Burns, Rhea Eskew, and Adam Reeves for helpful All experimental procedures were performed in accord with protocols comments. approved by the Institutional Animal Care and Use Committee at North- Correspondence should be addressed to either of the following: Frank Naarendorp, Department of Psychology, Northeastern University, 125 Nightingale Hall, 107 Forsyth Street, Boston, MA 02115, E-mail: f.naarendorp@ eastern University. Breeding pairs of wild-type (WT) C57BL/6 mice were neu.edu;orEdwardN.PughJr,CenterforNeuroscience,UniversityofCalifornia,Davis,1544NewtonCourt,Davis,CA purchased from Charles River Laboratories. Pups were born and raised Ϫ2 95616, E-mail: [email protected]. under cyclic lighting (12 h light/dark cycle with 1.5 photopic cd m DOI:10.1523/JNEUROSCI.2186-10.2010 light). The mice were at least 60 d old when they were first individually Copyright © 2010 the authors 0270-6474/10/3012495-13$15.00/0 moved to an experimental cage in which they would remain for months. 12496 • J. Neurosci., September 15, 2010 • 30(37):12495–12507 Naarendorp et al. • Mouse Rod and Cone Visual Sensitivity a c 15 10 5 Amplitude (mV) 0 0.0 0.2 0.4 0.6 0.8 1.0 1.2 Flash duration (ms) b Lensed LED d Neutral density filter Interference filter Light from target Translucent cage cover Opal diffusing glass Target aperture (max dia: 0.7 in) Line of sight 60o Dorsal retina IR emitter-detector Distance from target to bottom of wheel: 7.5 in Wheel dia: 5.0 in Retinal image Ventral retina of target Figure 1. Schematic of the “running mouse” apparatus and details of light calibrations.a, Photographs of the mouse cage. Left, A mouse is seen near the water spout extending from the wall on the lower left.TheblackcylindricalassemblymountedabovetherunningwheelcontainedanLEDthatprovidedthevariable-intensitylightflash(seeMaterialsandMethods).Right,Duringallexperiments,themousecage wasplacedinsideaninvertedtranslucentboxraisedslightlyabovethetabletopermitthefreeflowoffreshair;theboxalsoservedasalightdiffuserforexperimentsinwhichthemousewaslightadapted.b,Scale drawingoftherunningwheelandLEDlightsource,identifyingimportantcomponentsanddistances.IR,Infrared.c,SamplecalibrationtracesobtainedwithPINphotodiodelocatedatthebottomofthewheel at the level of the mouse’s eye; each trace represents one of the timed flashes delivered to the mouse’s eye on different trials. d, Magnified image of a mouse eye by Remtulla and Hallett (1985), as reproduced in (Lyubarsky et al., 2004), oriented with respect to the light field as it would be for a mouse on the lowermost position of the wheel. The cyclic lighting was then set for 18 h dark, 6 h light (1 cd m Ϫ2), and Geometry of the apparatus. Figure 1b presents a scaled diagram of the experiments were conducted during the nominally dark phase of the apparatus, identifying its principal components, including in particular cycle. The 18 h dark period gave the mice time to complete a sufficient the running wheel and light source. The light source consists of an inter- number (60–80) of trials in experiments that required the dark-adapted changeable, lensed light-emitting diode (LED) source mounted at a fixed state. During experiments requiring light adaptation, the background position in a light-proof, baffled black Lexan cylinder, which also contained light effectively extended the light cycle up to ϳ14 h, until the mice had a narrow band (ϳ10 nm) interference filter; one to three calibrated, absorp- completed 40–60 trials. tive neutral density filters; and a circumscribed opal diffusing glass window Seven male and five female C57BL/6 mice were used in experiments through which light exits (details of the LED sources are provided in supple- that measured their absolute sensitivity, the increment threshold re- mental Table S2, available at www.jneurosci.org as supplemental material). Ϫ/Ϫ sponse, or spectral sensitivity. Three Gnat1 mice, 3 to 4 months of Visual inspection and calibrations showed the diffusing window to act as a age, were kindly provided by Dr. Janis Lem (Tufts University, Boston, Lambertian source for the viewing angles at which the mouse would see it, cpfl3 MA). Six Gnat2 mice, three pigmented and three albinos (ALS/LtJ), 2 which range from approximately perpendicular to the source (mouse at the to 4 months of age, were generously provided by Dr. Bo Chang (The lowermost point of wheel) to ϳ30° from perpendicular (highest point on Jackson Laboratory, Bar Harbor, ME). wheel that the mouse reaches). The exposed
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