Abstract
The white noise electroretinogram (wnERG) provides a measure of the impulse response function under conditions of retinal equilibrium; it is yet to be determined how the electrical response generated by melanopsin ganglion cell photoreception is expressed in the impulse response. To this end, we recorded the human wnERG to continuous temporal white noise (TWN) stimuli that were melanopsin-directed (rod and cone silent) or cone-directed (rod and melanopsin silent). The impulse response of the electroretinogram was derived by cross-correlating the TWN stimulus with the wnERG response. We observed that the LMS-cone directed wnERG contained the expected N1 wave (24.1 ± 2.4 ms; mean ± SEM) and P1 wave (49.7 ± 1.8 ms). Melanopsin-directed stimuli produced a unique wnERG with a slower negative deflection (Nm) at 62.9 ± 3.3 ms followed by a positive deflection (Pm) at 126.3 ± 5.1 ms. Additional experiments indicated this melanopsin-directed wnERG response was not due to cone intrusion. The Nm and NmPm amplitudes increased with illuminance (32,000–80,000 Td; no rod intrusion) and melanopsin contrast (10–36% Michelson contrast). As there are known pathways connecting melanopsin cells to the outer retina, we then measured the wnERG to combined melanopsin and cone-directed stimuli to quantify melanopsin interactions with cone signalling. With the combined stimuli, the N1P1 amplitudes were suppressed by ~59%, which may be a result of a destructive interference between the positive (P1) and negative (Nm) waves generated by the cone and melanopsin pathways. We conclude that the human wnERG to melanopsin-directed stimuli may reflect the combined response of intra-retinal melanopsin pathways, independent of rod and cone photoreception.
Highlights
IntroductionMelanopsin-expressing intrinsically photosensitive Retinal Ganglion Cells (ipRGCs) mediate photoreception independent of conventional rod and cone photoreceptors (Berson, Dunn, & Takao, 2002; Dacey et al, 2005; Gamlin et al, 2007; Grünert, Jusuf, Lee, & Nguyen, 2011; Lucas et al, 2003; Nasir‐Ahmad, Lee, Martin, & Grünert, 2019) to regulate image forming (Cao, Chang, & Gai, 2018; Cao, Nicandro, & Barrionuevo, 2015; Horiguchi, Winawer, Dougherty, & Wandell, 2013; Spitschan et al, 2017; Zele, Adhikari, Cao, & Feigl, 2019b; Zele, Adhikari, Feigl, & Cao, 2018; Zele, Feigl, Adhikari, Maynard, & Cao, 2018) as well as non-image forming visual functions (Adhikari, Zele, & Feigl, 2015; Berson et al, 2002; Gamlin et al, 2007; Gooley et al, 2012; Kelbsch et al, 2019; Zele, Adhikari, Cao, & Feigl, 2019a)
In all 10 observers, the impulse response function (IRF) of the white noise electroretinogram (wnERG) measured with melanopsin-directed stimuli (Fig. 2A, green lines) had a negative deflection on average at 62.9 ± 3.3 ms followed by a positive deflection at 126.3 ± 5.1 ms
We present evidence that the melanopsin-directed wnERG gives rise to a waveform with negative (Nm) and positive (Pm) deflections (Fig. 2) that are ~39 ms and 77 ms slower than the cone wnERG N1 and P1 waves, respectively
Summary
Melanopsin-expressing intrinsically photosensitive Retinal Ganglion Cells (ipRGCs) mediate photoreception independent of conventional rod and cone photoreceptors (Berson, Dunn, & Takao, 2002; Dacey et al, 2005; Gamlin et al, 2007; Grünert, Jusuf, Lee, & Nguyen, 2011; Lucas et al, 2003; Nasir‐Ahmad, Lee, Martin, & Grünert, 2019) to regulate image forming (Cao, Chang, & Gai, 2018; Cao, Nicandro, & Barrionuevo, 2015; Horiguchi, Winawer, Dougherty, & Wandell, 2013; Spitschan et al, 2017; Zele, Adhikari, Cao, & Feigl, 2019b; Zele, Adhikari, Feigl, & Cao, 2018; Zele, Feigl, Adhikari, Maynard, & Cao, 2018) as well as non-image forming visual functions (Adhikari, Zele, & Feigl, 2015; Berson et al, 2002; Gamlin et al, 2007; Gooley et al, 2012; Kelbsch et al, 2019; Zele, Adhikari, Cao, & Feigl, 2019a). There are a few studies of the melanopsin contribution to the light-adapted photopic flash ERG, with evidence that the response is dependent on the recording conditions (Allen & Lucas, 2016; Fukuda, Higuchi, Yasukouchi, & Morita, 2012). Vision Research 164 (2019) 83–93 contribution to the ERG is evident as a series of positive and negative deflections after flash on– and off-set that are different to the conedirected ERG waveforms (Fukuda et al, 2012). Given this incongruity, the melanopsin contribution to the ERG is unclear
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