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The Transition from Scotopic to Photopic Vision in 3-Month-Old Infants and Adults: an Evaluation of the Rod Dominance Hypothesis

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The Transition from Scotopic to Photopic Vision in 3-Month-Old Infants and Adults: an Evaluation of the Rod Dominance Hypothesis Vision Research 40 (2000) 3853–3871 www.elsevier.com/locate/visres The transition from scotopic to photopic vision in 3-month-old infants and adults: an evaluation of the rod dominance hypothesis Sarina Hui-Lin Chien a,*, Davida Y. Teller a,b, John Palmer a a Department of Psychology, Uni6ersity of Washington, Box 351525, Seattle, WA 98195-1525, USA b Department of Physiology/Biophysics, Uni6ersity of Washington, Box 351525, Seattle, WA 98195-1525, USA Received 25 November 1999 Abstract The scotopic to photopic transition was tested in adults and 12-week-old infants using a large field motion nulling technique at a series of luminances between −3.57 and 2.70 log cd m−2. The stimuli were composed of 0.25 cyc deg−1, 5.6 Hz blue/black and yellow/black sinusoidal grating components, superimposed and moving in opposite directions. The contrasts of the two components were traded off to determine motion nulls at each luminance level. An eye movement based response measure was used for infant subjects, whereas self-report was used in adults. In both age groups, the motion null values approached a scotopic % l l asymptote consistent with V ( ) at the lowest luminance levels, and a photopic asymptote consistent with V10( ) at the highest luminance levels. The scotopic to photopic transition was gradual and occurred over about 3 log units between about −2 and 1 log cd m−2 in both groups. The null values for infants and adults were highly similar at each luminance level, and the shapes of the transition curves were virtually identical at the two ages. These data suggest that at each different luminance level, the balance between rod-initiated and cone-initiated signals in the extrafoveal luminance channel is similar or identical in 12-week-old infants and adults. © 2000 Elsevier Science Ltd. All rights reserved. Keywords: Infant vision; Infant color vision; Mesopic vision; Mesopic photometry; Motion nulling 1. Introduction 1.1. Adult mesopic 6ision The human eye changes its sensitivity to process In adults, scotopic vision is marked by a spectral scenes under a wide range of illuminations. One of the efficiency function that corresponds to the CIE scotopic most fundamental mechanisms for handling variations spectral efficiency curve V%(l). Photopic vision is more in illumination is the presence of two different kinds of complex, and different methods of measurement yield photoreceptors, rods and cones. The differential activa- different spectral efficiency curves. A range of tech- tion of rods and cones results in the three well known niques including heterochromatic flicker photometry ranges of vision, scotopic vision, in which rods function (HFP), minimally distinct border judgments (MDB) alone at low light levels; photopic vision, in which and motion photometry all yield spectral luminosity l cones function alone at high light levels; and mesopic functions closely resembling V( ), the spectral lumi- vision, in which both rods and cones function together nous efficiency function of the CIE standard observer. at intermediate light levels. The primary purpose of this All three of these techniques also display additivity. paper is to explore the transition from scotopic to These techniques stand in contrast to techniques of photopic vision with large field motion photometry in heterochromatic brightness matching (HBM), in which infant subjects, and to compare it to the same transition broader spectral curves are found, and in which match in adults. values are typically non-additive (for reviews see Poko- rny, Smith, Verriest, & Pinckers, 1979; Lennie, Poko- rny, & Smith, 1993). * Corresponding author. Tel.: +1-206-5439713; fax: +1-206- 6853157. In the transitional or mesopic range, in which both E-mail address: [email protected] (S.H.-L. Chien). rods and cones are active, spectral efficiency curves 0042-6989/00/$ - see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0042-6989(00)00200-5 3854 S.H.-L. Chien et al. / Vision Research 40 (2000) 3853–3871 shift from being consistent with V%(l) to being consis- cesses can proceed at least partially independently in l l tent with CIE V( ), V10( ), or other measures of pho- rod versus cone pathways. At the next stage of process- topic spectral efficiency. The mesopic range, which is ing, rod bipolar signals combine with cone-initiated usually studied with 10° test fields and heterochromatic signals via a rod bipolar/AII amacrine/cone bipolar brightness matching, is generally considered to extend circuit. As a consequence many ganglion cells receive over about 4 log units, from about −3 to about 1 log major inputs from both rods and cones. cd m−2 (Wyzecki & Stiles, 1982). However, the transi- Although the fit of psychophysics with physiology is tion is complex and labile, and the shapes of transi- not yet perfect, it is likely that the diffuse bipolars and tional spectral efficiency curves are affected by many the parasol ganglion cells provide the earliest neural factors including the method of measurement, spa- instantiation of a luminance channel receiving L, M tiotemporal parameters, field size, retinal location, and and rod input. The balance of rod and cone inputs the wavelength composition of the stimuli (e.g. Kinney, presumably trades off, from rod-dominated at very low 1964; Palmer, 1966, 1967, 1968; Ikeda & Shimozono, light levels to cone-dominated at very high light levels, 1978; Vienot & Chiron, 1992; Wyzecki & Stiles, 1982). with a continuously varying balance in between. In the In a recent and exemplary study, Vienot and Chiron present paper, we ask whether this balance is the same (1992) directly compared the results of flicker photome- in infants and adults, at each different light level across try and heterochromatic brightness matching through- the scotopic to photopic transition. out the full mesopic range. In their study, 10° test fields were used for both methods, and test wavelengths of 1.2. Scotopic, mesopic, and photopic 6ision in infants 445, 560, and 630 nm were compared with 3780 or 3850 K white. The subject was allowed to adjust the flicker The term Purkinje shift is classically used to define rate in the flicker measurements. Vienot and Chiron the change in the apparent brightnesses of short- versus found that heterochromatic brightness matching pro- long-wavelength lights at dawn or dusk, brought about duces a very gradual scotopic to photopic transition. by the shift between scotopic and photopic vision The mesopic range covered over 2.5 log units for (Pokorny et al., 1979). In two early studies of infant short-wavelength lights and 4 log units or more for spectral sensitivity, Peiper (1926) and Trincker and long-wavelength lights, in agreement with the previous Trincker (1955) used the ‘eye-on-the-neck reflex’ — literature. In contrast, flicker photometry produced a probably a startle response — to measure spectral much more abrupt transition, covering 1 log unit or sensitivity in newborn infants under photopic and sco- less. In some cases the transition was even discontinu- topic conditions. Although the stimuli are not well ous, with the flicker match jumping from a nearly defined by modern standards, the data nonetheless scotopic to a nearly photopic value at a single mesopic clearly demonstrate a Purkinje shift. These early studies luminance as the subject changed the flicker rate from suggested that both scotopic and photopic mechanisms low to high. The sharp transition or discontinuity oc- are functional in young infants. curred in the middle of the mesopic range defined by In a more modern study of scotopic spectral sensitiv- heterochromatic brightness matching. ity, Powers, Schneck, and Teller (1981) used forced- In classical psychophysical theory, the signals from choice preferential looking (FPL) to measure the dark the photoreceptors are presumed to be recombined to adapted infant’s sensitivity to spectral lights between yield three postreceptoral channels — a luminance 410 and 649 nm. With respect to adult absolute channel and two chromatic channels (Jameson & Hur- thresholds, infant absolute thresholds were elevated by vich, 1955; Boynton, 1979; Krauskopf, Williams, & about 1.7 log units in 1-month-olds and 1 log unit in Heeley, 1982). The signal in the foveal luminance chan- 3-month-olds. Spectral sensitivity in 1- and 3-month nel is believed to be formed from a weighted linear sum olds matched the CIE scotopic luminosity function at of inputs from L- and M-cone-initiated signals. all wavelengths longer than 430 nm, with suggestions of Mesopic and extrafoveal spectral efficiency functions increased sensitivity at the shortest wavelengths. When have been modeled with various combinations of sco- VEP techniques are used, similar but smaller elevations topic and photopic inputs, with weights that vary with of absolute thresholds are found (Hansen & Fulton, the luminance level (e.g. Palmer, 1967, 1968; Ikeda & 1993). Werner (1982) showed good agreement between Shimozono, 1981; Yaguchi & Ikeda, 1984; Sagawa & V%(l) and the infant’s spectral efficiency curve in the Takeichi, 1986). mid-wavelength region. Infants’ sensitivities were In physiological terms, the postreceptoral channels clearly elevated at the shortest and longest wavelengths. are believed to be formed within the retina (Boynton, These elevations are attributed to a reduced lens density 1979; Dacey & Lee, 1994). L- and M-cone-initiated in infants, and the intrusion of L-cone-initiated signals, signals are combined at the horizontal and cone bipolar respectively (Werner, 1982; Hansen, & Fulton, 1993). cells, whereas rod-initiated signals are processed largely These results clearly establish the presence of a func- by the rod bipolars. Thus, early light adaptation pro- tional scotopic mechanism in very young infants. S.H.-L. Chien et al. / Vision Research 40 (2000) 3853–3871 3855 In the case of photopic spectral sensitivity, the earli- short- to middle-wavelength range (cf. Gordon & est modern investigations were carried out with non- Abramov, 1977).
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