Color vision of people with headaches

Griber Yuliya Alexandrovna Doctor of Cultural Studies Professor, Director of Color Laboratory at Smolensk State University 214000, Russia, Smolensk region, Smolensk, Przhevalskogo str., 4 y.griber@gmail.com Other publications by this author     Delov Aleksey Alekseevich ORCID: 0000-0001-8589-8523 Researcher at the Color Laboratory of Smolensk State University 214000, Russia, Smolensk region, Smolensk, Przhevalsky str., 4 aleksejdelov@gmail.com

Kovalev Pavel Sergeevich ORCID: 0000-0002-1223-8812 Researcher at the Color Laboratory of Smolensk State University 214000, Russia, Smolensk region, Smolensk, Przhevalsky str., 4 rozdavid2009@yandex.ru

Introduction

Headaches in the modern world are among the most common diseases of the nervous system. According to epidemiological studies, 62% of Russian residents suffer from recurrent headaches ^[1] and about 50-75% of the adult population of the entire Earth ^[2]. Despite some regional differences, headaches are a global problem affecting people of all races, income levels and geographical regions ^[3].

People experiencing headaches constantly report similar visual triggers that can cause them to have a new attack. Certain visual qualities of the environment have a noticeable effect on their well-being (see appendix: ^[4]). Among the most significant are certain characteristics of natural and artificial lighting ^{[5; 6]}, flickering light ^[7], certain visual images ^[8], the specific structure of the interior space of premises and workplaces ^[4].

Awareness and avoidance of these and other provoking factors is important not only in comprehensive headache treatment programs as part of a therapeutic regimen, but also in designing a "liveable" environment (see research review: ^[9-11]). Therefore, over the past few decades, clinical specialists and scientific researchers have been studying with special interest the relationship of various aspects of headache with individual components of the visual system.

Special attention is paid to the parameters of visual discomfort, which is sometimes called "visual stress" or simply "sensitivity" (to patterns, glare, colors, etc.) (see e.g.: ^[12]). The interest in this issue is largely explained by the fact that there seems to be a connection between the visual triggers of headache and the feeling of visual discomfort. As a rule, people who are susceptible to visual headache triggers also experience greater discomfort when viewing trigger stimuli ^{[13; 14]}.

The data already obtained also indicate that there is a connection between visual discomfort and color sensitivity – the ability to perceive different shades of color with different spectral composition of radiation (see e.g. ^[15]). At the same time, the theory of efficient coding is gaining increasing empirical support ^[12], according to which visual stress is caused by shades that differ significantly from the usual ones – those that are usually found in the natural environment surrounding a person (see appendix: ^[16]).

Studies show that in people suffering from headaches, color sensitivity does not coincide with the age-appropriate control group. The differences relate to the perception of pink ^[8], red ^[17], blue and purple shades ^[18]. Some groups of bright shades (primarily saturated and intense red and orange) are strong visual triggers for patients with chronic headaches that can provoke a new attack ^[7].

The effect of tinted lenses on the feeling of visual discomfort and the frequency of headaches has also been established. In particular, subjects who constantly wore glasses with colored lenses were less likely to have headaches compared to participants from the control group ^{[5; 19]}. A similar corrective effect on the feeling of visual discomfort was also provided by a colored background for a computer screen [13)].

At the same time, a review of the works published so far proves that the analysis of color sensitivity in people with headaches, in the vast majority of cases, is limited to patients with migraines (see, for example.: ^{[7; 8; 13; 14; 17; 18]}). As far as we know, comprehensive studies of color perception in people with other types of headaches have not yet been conducted. Only a few isolated cases of specific color sensitivity in people with cluster headaches have been described ^{[5; 19]}.

In this article, we will continue to study the specifics of perception of chromatic environmental parameters and color sensitivity. The purpose of the article is to obtain new data on possible changes in color vision in people with primary headaches. According to statistics, primary headaches account for 95-97% of all cases ^[20]. Unlike secondary (symptomatic) headaches, they are characterized by the absence of organic damage to the brain, head and neck structures. The most well-known form of primary headaches is migraine. However, at the same time, it is by no means the most common and in Russia accounts for only 14% of all cases. Along with migraine, primary headaches include many other forms, including tension headache, trigeminal autonomic cephalgia, cough pain, headache associated with physical exertion, sexual exertion ^[21].

The hypothesis of the study is that in people experiencing recurrent primary headaches of different nature, the perception of chromatic environmental parameters and color sensitivity changes; differences may correlate with the experience of headaches, the frequency of their occurrence, the nature and quality of the pain experienced, their intensity and localization.

Research materials and methods

(1) Participants

The study involved 65 people (13 men and 52 women) aged 17 to 66 years (average age 26.3, SD=12.1). All of them have recently experienced headaches of varying intensity, nature and quality, which they experienced with varying frequency. On average, the experience of headaches was 10.64 years (minimum – 1 year, maximum – 46 years, SD=10.10).

The results of the assessment of color vision in the experimental group were compared with the normative indicators ^[22-24] and the data obtained in the age-matched control group (N=40, average age 23.54, SD=8.4, 12 men and 28 women). All study participants had normal or normalized visual acuity.

Before starting the study, each of the participants independently filled out a detailed questionnaire that included an expanded set of questions about various aspects of headaches. The questions concerned the temporal pattern of headaches (time from the moment of the first and last attack, duration and frequency of attacks), the nature, quality and intensity of pain, established triggers, and the presence of accompanying symptoms.

(2) Color vision assessment procedure

Data collection was carried out using the standard clinical Farnsworth-Munsell color vision test for 100 shades (Farnsworth-Munsell 100-hue test, FM-100) ^{[25; 26]}. In the practice of scientific and clinical research, this test is traditionally used to diagnose the type and severity of acquired color vision disorders caused by various pathologies of the visual system (including maculopathy, glaucoma, optic neuritis, cataracts), systemic diseases (such as diabetic retinopathy or hypothyroidism), as well as the influence of various kinds of extreme changes in the environment the environment affects human visual perception (for example, by an extreme decrease in natural light beyond the Arctic circle) (see research review: ^[27]).

The FM-100 test contains 85 shades, which together form a complete color circle. The shades are separated by approximately equal perceptual steps. They differ only in tone and have the same lightness and saturation (Value 6 and Chroma 6 in the symbols of the Mansell system).

The chips are stored in four pencil cases, which are often designated with the Latin letters A, B, C and D. There are 22 chips in pencil case A, and 21 in the other three. In each of the four pencil cases, the chips represent a certain sector of the color circle: from red to red-orange (pencil case A, chips 85-21), from yellow to yellow-green (pencil case B, chips 22-42), from green to green-blue (pencil case C, chips 43-63) and from indigo to magenta (pencil case D, chips 64-84). The extreme chips in each of the pencil cases are fixed, the rest are movable.

Each participant in the study was asked to arrange the chips in the pencil cases in such a way that the transition from one shade fixed at the end of the pencil case to the other was as smooth as possible. In accordance with the recommendations for people with neurological disorders (see, for example: ^[18]), the time for completing the task was not limited.

(3) Data analysis

The data was analyzed using specialized computer programs. The analysis included calculating the total error (TES) and calculating partial errors (PES) along the blue-yellow (B-Y) and red-green (R-G) axes. Partial errors for individual tones were also calculated.

(3.1) Total Error (TES) is an indicator that is used to assess the quality of color differentiation in general. It is calculated as the sum of the points for the chips in the four boxes. The score for an individual chip is calculated as the sum of the absolute difference between the error value for a given color and the error values of neighboring chips minus 2 ^[26]:

,

where i is the number of the pencil case; Cj is the number of the chip j; CEj is the error of the chip j; n is the number of movable chips in the pencil case corresponding to i (n = 22 for pencil case A, and n = 21 for pens B–D).

If all the chips are in the correct order, the value of the total error TES =0; the more offsets the chips, the higher the TES score.

Since TES has an asymmetric distribution, calculations often use the square root of the total number of errors (√TES) to obtain a distribution closer to normal ^[24].

(3.2) Partial errors (PES) were calculated for individual shade ranges:

(1) along the axes:

blue-yellow B-Y axis (chips 1-12, 34-54 and 76-85);

red-green R-G axis (chips 13-33 and 55-75);

(2) for individual tones:

from red to yellow-red R-YR (chips 1-9);

from yellow-red to yellow YR-Y (chips 10-17);

from yellow to yellow-green Y-GY (chips 18-26);

from yellow-green to green GY-G (chips 27-35);

from green to blue-green G-BG (chips 36-45);

from blue-green to blue BG-B (chips 46-53);

from blue to blue-purple B-PB (chips 54-60);

from blue-purple to purple PB-P (chips 61-70);

from purple to purple-red P-RP (chips 71-77);

from purple-red to red RP-R (chips 78-85).

Results

General Error (TES)

In the majority of patients experiencing headaches (80%), color vision corresponded to their age norm (Table 1). In 11 participants (17%), the value of the total number of errors exceeded the average value for healthy normal trichromates, but it was still within the upper limit. Only two people (a woman, 19 years old, and a man, 25 years old, both experience frequent headaches) had slightly worse color vision than normal (√TES=10.58 and √TES=9.59, respectively).

Table 1. The mean value and standard deviation of the square root of the total number of errors (√TES) for healthy normal trichromates, presented in ^{[22, Table 1],[23, Table 1]}) and ^{[24, Table 1]}

We found a positive correlation between the frequency of headache occurrence (episodic, frequent, chronic) and the value of the total error score (√TES) (Fig. 1). On average, this indicator in people with episodic pain was 4.18 and turned out to be even lower than in the control group, where √TES=4.92. In people experiencing frequent and chronic pain, the magnitude of the total error (√TES) was noticeably higher and amounted to 5.51 and 5.83, respectively.

Fig. 1. Correlation between the frequency of headache occurrence (episodic, frequent, chronic) and the value of the total error score (√TES)

The correlation between the magnitude of the total error score (√TES) and the intensity of the headache was also even more significant. In patients with mild, moderate and severe headaches, this indicator was 3.89, 4.54 and 6.53, respectively (Fig. 2).

Fig. 2. Correlation between headache intensity (mild, moderate, severe) and the value of the total error score (√TES)

In addition, the value of the total error score (√TES) correlated with the localization of headaches. In patients with localized pain, this indicator was lower on average than in patients who experienced pain without a specific localization (√TES=4.65 and √TES=5.56, respectively).

We did not find a statistically significant correlation between the experience of headaches and the value of the total error score (√TES) (Fig. 3).

Fig. 3. The function of headache experience and the value of the total error score (√TES)

The correlation of the total error score (√TES) with age, gender, nature and quality of headaches (aching, pressing, throbbing, acute, bursting), normal behavior during an attack (drowsiness, emotional arousal, anxiety, fear) and heredity of headaches also turned out to be statistically insignificant.

Partial errors (PES) along the blue-yellow and red-green axes

In patients with frequent (from two to ten attacks per month) and chronic (more than ten attacks per month) headaches, errors along the blue-yellow (B-Y) axis prevailed among partial errors (√PES) (Fig. 4). In patients with frequent pain, the average value of √PES (B-Y) was 4.07; the average value of √PES (R-G) was 3.53. In patients with chronic pain, the average value of √PES (B-Y) reached 4.43; the average value of √PES (R-G) was 3.50.

Fig. 4. Partial errors (√PES) along the blue-yellow (B-Y) and red-green (R-G) axes in patients with different frequency of headaches

A similar pattern was found in participants with moderate to severe pain (Fig. 5). In subjects with moderate pain, the average value of √PES (B-Y) was 3.27; the average value of √PES (R-G) was 2.86. In patients with severe pain, the average value of √PES (B-Y) It reached 4.96; the average value of √PES (R-G) was 4.07.

Fig. 5. Partial errors (√PES) along the blue-yellow (B-Y) and red-green (R-G) axes in patients with different headache intensity

A similar predominance of errors along the blue-yellow axis was also described in the study by A. Shepherd ^[18] for people with migraine. However, in this experiment, the difference with the red-green axis turned out to be statistically insignificant, and the relationship between the frequency of pain, their intensity and nature was not recorded.

In the control group, such a difference between the number of errors along the blue-yellow and red-green axes was statistically insignificant: the average value of √PES (B-Y) was 3.49; the average value of √PES (R-G) was 3.21.

Partial errors (PES) for individual tones

The most noticeable increase in the number of errors, compared with the control group, was recorded in patients experiencing frequent and chronic pain for blue-green and blue shades (BG-B).

Fig. 6. The average value of the partial error (Mean PES) for individual tones in patients with different frequency of headaches (green lines) and in the control group (red line)

The number of errors for individual tones was also correlated with the intensity of headaches. In patients experiencing severe pain, there was a noticeable increase in the number of errors in the range from green to blue (G-BG and BG-B) (Fig. 7).

Fig. 7. The average value of the partial error (Mean PES) for individual tones in patients with different headache intensity (blue lines) and in the control group (red line)

Patients with non-localized headaches made more mistakes in the green, blue-green, blue and purple-red hue ranges compared with the control group and with study participants whose pain was localized (Fig. 8).

Figure 8. Mean partial error (Mean PES) for individual tones in patients with varying degrees of headache localization (gray lines) and in the control group (red line)

Discussion and conclusions

The study showed a noticeable specificity in the perception of blue-green and blue shades in patients with severe, chronic and non-localized headaches.

The most significant changes in color perception were noted for blue shades in subjects with chronic pain. All of these people experience more than 10 seizures per month and experienced the last attack a few days before the start of the study. Based on this frequency, we can assume that the color discrimination disorder noted in them could not be a consequence of an attack suffered before the start of testing, but a predictor of a new one. A similar violation of the perception of blue in the premonitory phase was noted in other previously conducted experimental studies of migraine, according to which a reduced perception of blue was observed only in patients who experienced an attack within 72 hours immediately after testing ^[17].

To date, there is no clear answer to the question of the causes of color vision disorders in people suffering from headaches. Color differentiation is a complex process involving retinal, subcortical and cortical components. At the lowest level of visual signal processing, light is absorbed by three cone photoreceptors of the L-, M- and S-type, which respond to long (or red), medium (green) and short (blue) waves, respectively. In the retina, the signals are converted into two opposing channels L ± M (red-green) and S-(L + M) (blue-yellow). The antagonism of cones persists in the retinofugal visual pathways at least up to the primary visual cortex (V1). The presence of these two channels leads to the appearance of two physiologically important sets of colors in any color space. These colors form the so-called "cardinal" color directions, since in each case they stimulate one and only one cone-shaped pathway connecting the retina and cortex (see e.g.: ^[13]).

To assess the sensitivity of the cone photoreceptors of the retina, the calculation of the number of errors along the blue-yellow and red-green axes is traditionally used. When perceiving shades along the blue-yellow axis, only the signal from the S-type cones changes, the signals from the L- and M-cones remain constant. Along the red-green axis, on the contrary, the signal from the S-cones remains unchanged, but the ratio of activity of the L- and M-cones changes. Accordingly, the partial error indicator along the blue-yellow axis (PES(B-Y)) allows you to evaluate the sensitivity of S-type cones, along the red-green (PES(R-G)) – the sensitivity of L- and M-cones.

In our study, it was found that the differences in color perception between the group with headaches and the control group mainly relate to the blue-yellow axis, i.e. they are limited to shades selective for S-type cone photoreceptors. In previous studies, no differences were found for shades selective for L- and M-type cones (see sub-section: ^[18]). Patients with migraine examined between attacks had a similar deficiency in sensitivity to short wavelengths ^[28].

The revealed changes in color perception hardly reflect changes in the work of the retina or photoreceptors. Since the decrease is limited exclusively to one group of shades, it most likely occurs at the precortical stage or at the stages preceding the unification of signals from cone-opponent signals (cf.: ^[18]).

Similar disturbances in the perception of blue color are characteristic of the early stages of diseases with retinal dysfunction, such as glaucoma and diabetes, while impaired perception of red color seems to be more common in diseases with damage to the foveal region (see appendix: ^[17]).

On the other hand, there is some reason to assume that the detected disorders may be related to the work of the dopaminergic system. Studies show that this system is directly related to headaches and migraines ^[29]. In particular, a migraine attack may be preceded by precursor symptoms, which are believed to be associated with dopaminergic dysfunction. These symptoms, which may occur 3 days before the attack and earlier, include changes in mood, behavior, alertness, appetite and intestinal activity (see appendix: ^[17]). In light of these observations, the decrease in blue color perception that we observed in patients with chronic headaches shortly before an attack may be an expression of the precursor phase of the attack, which is characterized by dopaminergic dysfunction.

This interpretation may be consistent with clinical evidence that impaired perception of blue color is also noted in Parkinson's disease ^{[30; 31]}. At the same time, it is suggested that in such patients, an acquired defect in the perception of blue color may originate at the retinal level, since in Parkinson's disease dopaminergic neurons can degenerate both in the retina and in the brain stem.

Since the detected color vision disorders appear to be temporary and are most likely typical of the premonitory phase of seizures, the results of this study may contribute to further study of predictors of headache.

The new data obtained on changes in color vision may be useful for understanding not only the pathophysiology of headache. Since the identified changes relate to only one group of (blue) shades, the findings of the study can be used in the development of alternative treatment methods. In particular, to choose the optimal color of tinted lenses, which are offered to patients to relieve headaches and reduce the frequency of seizures ^{[5; 19]}.