1. Introduction
Visual Acuity is the widespread test to evaluate visual function [
1]. However, contrast sensitivity, stereopsis, color perception and temporal vision are also important factors of visual function that are frequently relegated in clinical practice [
2]. The temporal aspects of vision are mainly visual latency [
3], perisaccadic compensation, persistence [
4], temporal integration [
5] and resolution [
6].
Time perception is also influenced by non-temporal aspects such as contrast and orientation of the visual test [
7]. Visual persistence can be understood as prolonged visual perception for a short time after the physical stimuli is removed. From the point of view of retinal physiology, visual persistence is due to light-adaptive gain control mechanisms in the response of ganglion cells [
8].
The perception of objects in motion requires the integration of spatiotemporal information [
9]. In this sense, the temporal integration window (TIW) deals with the duration of a stimulus to be perceived with a duration of a single instant. Stimuli presented in sequence within a TIW of around 40 milliseconds are integrated into a single visual perception. Larger TIWs allow for temporal resolution and then the subjective perceptual experience of motion [
10]. Cortical visual impairment [
11] (CVI) affects processing functions in the temporal, parietal and frontal lobes of the brain, one of the CVI characteristics is the slow visual response when a visual target is presented, this delayed response is called visual latency and could require suprathreshold stimuli to achieve a visual response [
12].
The common way to measure the temporal resolution of visual performance is the Critical Flicker Frequency Fusion (CFF), which is the measurement of the temporal frequency of a periodically modulated flickering light at which the stimuli cannot be distinguished at any modulation amplitude [
13].
Its experimental simplicity has made the CFF the most evaluated representative temporal aspect of the visual function [
14]. CFF has been reported as a potential functional measure of temporal vision in multiple sclerosis [
15,
16,
17], retrobulbar neuritis [
18], demyelinating optic neuritis [
19] or cognitive performance [
20,
21].
Spatial resolution and color vision are mediated by cone photoreceptors that encode information for blue-yellow (B/Y) and red-green (R/G) channels and luminance through different cortical mechanisms [
22,
23]. Furthermore, the R/G and B/Y components combine for spatiotemporal modulation of color vision [
24]. In this sense, patients with degenerative retinopathy suffer from color vision impairment that can be examined psychophysically with chromatic CFF tests. Gregori et al., [
25] found altered CFF values for red light in patients with optics neuritis and impaired CCF for blue stimuli in patients with diabetic retinopathy.
In addition, the trichromatic (red, green and yellow) CFF was proposed as a visual test to discriminate between cataract patients with and without macular affection [
26]. The finding revealed a greater sensitivity in yellow-CFF to identify macular diseases.
Prior to this work, an Arduino-based LED stimulation device was reported for cognitive research in rodent models and heterochromatic flicker photometry in humans [
27]. Taking into account the relationship between retinal and post-retinal vision disorders and color vision impairment, the objective of this work is to present new a portable and cost-effective Arduino-powered device for the assessment of the chromatic critical flicker frequency fusion. The device allows the subjective evaluation of the CFF of almost any possible RGB combination and has been tested in 30 young adult volunteers. A new experimental psychophysical phenomenon related to the Talbot-Plateau law is observed: at a given flicker frequency in sequential sampling of red, green and blue colors, a continuous white light stimulus is perceived. In addition, ocular wavefront measurements revealed that high-order aberrations improve the temporal resolution of vision.
4. Discussion and Conclusions
This study presents a new cost-effective portable mini-device for trichromatic temporal resolution assessment of the human vision powered by Arduino technology. The use of pulse-width modulation (PWM) signals to control the brightness and flicker frequency of LEDs controlled by Arduino devices, may raise questions about possible limitations with respect to the use of other technologies based on data acquisition cards (DAQs). However, previous works have reported accurate irradiance output [
27] and timing precision of the LEDs based on PWM signals [
35]. Those precision tests demonstrated the reliability of using Arduino boards for psychophysical experiments. In contrast, cost-effective LED driving Arduino-based systems can be controlled using open-source programming environments. Additionally, Arduino devices are based on open hardware processors that can be modified by the user to extend the main capabilities of Arduino or to communicate multiple boards wirelessly.
Teiraki et al. [
27] reported a LED-based visual stimulator driven by an open-source Arduino microcontroller. Among other interesting applications, they demonstrated an application to measure the density of ocular media in humans based on heterochromatic flicker photometry.
Here a new setup demonstrates an application for assessing the temporal resolution of visual performance using a flickering trichromatic stimulus. CFF was measured for the individual red, green and blue channels and for white light. The highest CFF threshold for green light was found to be significantly higher than for red light.
Regarding the cCFF, the integration frequency was significantly higher than the rest of the color stimuli. That is, while the visual perception of flickering of a monochromatic stimulus would disappear, a trichromatic stimulus flickering at the same frequency would continue to be visible.
Considering the association between the human visual perception of high-frequency flicker stimuli with cortical mechanisms [
36], exploring the human visual perception of trichromatic flicker at higher temporal frequencies could help better understand the outcomes of psychophysical tasks and isolate those contributions from the magnocellular pathway.
Section 3.2 explored the relationships between the chromatic temporal resolution of the visual system and macular function measured by photo-stress recovery time (PRT).
No relationships were found between CFFs for red, green, blue light, cCFF and PRT. However, a statistical negative correlation was found between the red/green modulation contrast and PRT. Theoretically, the presence of macular pigment is to enhance the visual performance in glare vision conditions [
37]. In that sense, a higher macular pigment density will results in shorter PRTs. The results reported here showed that PRT and cCFF are independent factors of the visual function. Therefore, the contrast modulation parameter defined for red and green CFF measurements appears to be related to the macular pigment density rather than temporal processing of color vision.
Finally,
Section 3.3 studied the influence of ocular aberrations on the chromatic CFF. No relationships were found between cCFF and low-order aberrations (i.e., refractive errors), however a positive linear correlation was found between HOA and cCFF. The results demonstrate that high-order ocular aberrations improve the temporal resolution of the visual function.
Spatial contrast sensitivity and HOA are inversely correlated; One of the main mechanisms that degrade visual quality in corneal diseases such as keratoconus is the presence of increased HOA [
38]. Furthermore, HOA plays a compensatory mechanism in spatial contrast sensitivity when intraocular scattering effects are also significant [
39]. However, the influence of ocular aberrations on temporal aspects of vision is lacking in the literature.
A possible explanation for the relationship between HOA and cCFF can be found in the spatiotemporal mechanisms in human vision processing: spatial and temporal information interact with the magnocellular and parvocellular pathways, respectively. More specifically, there is an inhibitory parvo-magnocellular interaction: improving temporal resolution deteriorates spatial resolution [
40]. Therefore, it can be concluded that while on the one hand HOA degrades the optical quality of the eye (in terms of spatial resolution), on the other hand it improves the temporal resolution.
Recently, it has been reported that the human visual cortex is sensitive to flicker stimuli that induce changes in neural activity [
41]. In neurodegenerative diseases such as Alzheimer’s, the brain undergoes from electrophysiological changes that are susceptible to reacting to neurostimulation therapies based on chromatic flickering at 40 Hz [
42]. One of the drawbacks of studying brain activity with perceived flickering is a high level of patient discomfort [
43]. The results reported here showed a mean value for cCFF of 37.76 ± 14.03 Hz, then a trichromatic flicker stimulus at 40 Hz falls inside the steady perceived stimuli regime according to the Talbot´s law, allowing brain activity to be studied at that critical frequency while the patient looks at a continuous white visual stimulus.
To conclude, a new cost-effective mini-device for the study of polychromatic temporal resolution of visual function based on Arduino technology is presented. The cCFF device allowed us the study of the critical flicker fusion of a chromatic stimulus, providing a steady white visual perception beyond the critical frequency limit. The contrast modulation of CFF values for red and green stimuli was found to be related to photo-stress recovery time and therefore more related to macular pigment density than to temporal resolution of color vision. Furthermore, increased ocular HOA improves the temporal resolution of the visual function.
Future work will include characterization of the temporal sensitivity of color vision using the chromatic CFF device in patients with retinal visual impairment.