Skin reflectance, iris pigmentation and information processing in children

Physiology & Behavior, Vol. 27, pp. 255--259. Pergamon Press and Brain Research Publ., 1981. Printed in the U.S.A.

Skin Reflectance, Iris Pigmentation and Information Processing in Children H E L E N M. F L O Y D A N D M. G. K I N G

Department of Psychology, The University of Newcastle New South Wales 2308 Australia R e c e i v e d 1 D e c e m b e r 1980 FLOYD, H. M. AND M. G. KING. Skin reflectance, irispigmentation and infi~rmationprocessing in children. PHYSIOL. BEHAV. 27(2) 255-259, 1981.--Forty children 8 years of age were selected for either high (>54%) or low (<53%) skin reflectance, a variable previously noted to be influenced by a-Melanocyte stimulating hormone (a-MSH). To control for apparent inherited type of melanin density, iris pigmentation was included as a second independent variable, and the design crossed to obtain eight groups of children, representing all combinations of both high and low skin reflectance, light and dark iris pigmentation and sex. Tests of attention reported as sensitive to the infusion of a-MSH in human adults were administered. Auditory Continuous Performance Tests indicated no differential performances between groups. In contrast, Visual Information Processing Tests elicited superior performances from groups with low skin reflectance and more consistently from sub-groups of these with light iris pigmentation, indicating the concurrence of facilitation of the skills with the pigmentary changes previously noted on administration of a-MSH. Skin reflectance

Iris pigmentation

Visual attention

BEHAVIORS such as reversal learning and dimensional shifts have been found sensitive to the administration of a-MSH. MSH-treated animals acquire reversal responses significantly faster than controls, with an additional finding that the effect was enhanced in attentionally deficient rats such as those tested under constant illumination, and albino strains [19]. Selective attention then became the most viable explanation for these behavioral results [19]. The attention paradigms applied to human subjects include those testing the extra- and intra-dimensional shift, using color-form and weight-length, two-choice discriminations. On that task Sandman, George, Nolan, Van Riezen and Kastin [17] found that infusion of the active sequence MSH/ACTH 4--10 resulted in improved intra-dimensional shift and poorer extra-dimensional shift learning when compared with controls. A more sensitive test of visual information processing was applied by Sandman, George, McCanne, Nolan, Kaswan and Kastin [16] which broached, as well as selective attention, the question of threshold for the detection of low luminance stimuli implicit in the neurophysiological actions of the peptide. Attention was measured in two stages: detection (or simply perceptual threshold) and discrimination (processing ability of detected stimuli) using the paradigm evolved by Kaswan and Young [10]. Three levels of luminance were tested and in simple detection the experimental subjects exhibited impaired performance on low luminance stimuli. The discrimination tasks revealed a superior performance under treatment with MSH/ACTH 4-10. These findings indicated raised thresholds and improved visual stimulus processing following administration of the peptide. Sandman, George, Walker and Nolan [18] reported

Discriminability

enhancement of attention, both behaviorally and electrophysiologically in mentally retarded subjects, using the tests previously applied to normals. Attention in the form of sustained vigilance has also been investigated successfully in 'petit-mal' epilepsies [12], schizophrenias [13], and hyperkinetic children [20], by the use of the Continuous Performance Test (CPT). Bakay Pragay, Mirksy, Fullerton, Oshima and Arnold [1 ] employed intra-cerebral stimulation of sites in the macaque brain stem with simultaneous CPT measures to investigate loci of stimulation-induced errors of omission. These loci were found to be confined to the mesencephalic and pontine reticular formations, the pre-tectal area, pons, and red nucleus. Stimulation of the mesencephalic-pontine junction of the reticular formation produced reduction in amplitude of visual-evoked responses, and cessation of ongoing oculomotor activity typical of the'staring spell' of'petit-real' epilepsy. Thus, certain brainstem structures may be regarded as mediators of sustained attention particularly in the visual modality. Considerable evidence exists of the actions of a-MSH on brain stem structures and, albeit indirectly, on the visual cortex. The dorsal brainstem of the rat was found to respond to the administration of t~-MSH with decreased oxygen consumption [14]. Goldman, Skelley, Sandman, Kastin and Murphy [5] found a decrease in the rate of cerebral blood flow in all areas except the visual cortex of a-MSH treated rats. Christensen, Harston, Kastin, Kostrzewa and Spirtes [2] reported elevated levels of cyclic-adenosine monophosphate (cAMP) in the occipital cortex of both intact and hypophysectomized rats, with less robust effects evident in brainstem structures. It is of interest that intracerebral stimu-

C o p y r i g h t © 1981 Brain R e s e a r c h Publications Inc.--0031-9384/81/080255-05502.00/0

256

Fl,()'r D AND KIN(~

lation of brain stem sites, and the administration of o~-MSH can elicit opposing effects on attention and visual information processing. Melanocytes occur chiefly in the epidermis, the retinal pigment epithelium, the uveal tract of the iris and the leptomeninges. They derive embryologically from the neural crest, migrating as melanoblast to these sites [3]. The autogenetic activity of the melanocyte varies in each site. Tyrosinase activity, an indicator of melanogenesis, ceases in the retinal pigment epithelium at birth, in the uveal tract it is complete in early childhood, and in the epidermis melanin synthesis and dispersion continues into adulthood [3]. The variation in perceived depth of pigment depends on the degree of melanisation of granules in the melanocyte, a trait which is determined genetically, the degree of oxidisation of the melanin occurring on exposure to ultraviolet light, and upon the age-dependent degree of dispersion of the melanin granules. Elevated endogenous levels of c~-MSH, and ACTH are known to produce deepening of epidermal pigment, e.g., in Addison's disease and pregnancy [3]. c~-MSH causes hair follicle melanocytes of the siberian hamster to respond with increased melanogenesis in moult season [21]. It is suggested therefore that a comparison of inherited pigment evident in the iris colouration, with the development of epidermal pigment intensity, measured as skin reflectance, can operate as an indicator of the degree of melanotrophic activity. Melanin dispersion has been associated with neural transmission characteristics, in relation to threshold phenomena [111. The aim of the present study was to examine indirectly the influence of a - M S H on the development of visual information processing, in particular, and attention more generally, by relating these to age-dependent indices of melanocyte density and melanin dispersion measured as skin reflectance. The tests were applied to visual and auditory modalities in order to examine the hypothesis of general attentional enhancement. The visual paradigm of Kaswan and Young [10] used in the studies of Sandman et al. [16] was preferred for threshold measures. In the interests of time, and in consideration of the age of the subjects, however, luminance measurers were replaced by contrast measures. Auditory attention was measured by means of an auditory adaptation of the CPT. METHOD

Forty subjects were selected from groups of 8 year old pupils of three elementary schools according to the following attributes: (1) Skin reflectance measures were obtained from the forearm, medial aspect immediately distal to the elbow, using an Evans Electroselenium Spectroreflectometer. Subjects were selected from both extremities of the obtained range. (2) Iris coloration was observed under normal indoor ambient light (1.3935 lux) and categorized as follows: Light--blue, grey, green; Medium--grey-hazel, hazel, light brown; D a r k ~ a l l other browns. Subjects were selected as far as possible from the extremities of the range. The two variables were crossed to obtain four groups, with equal representation of sexes in each. All subjects underwent the following two tests of visual and auditory attention and information processing with the order of presentation of the two tests randomized. Visual Low Contrast Detection and Discrimination This test consisted of 80 slides, 40 of which were blank

(noise) and 40 of which contained either "t!i or '1-' at two, possible contrast levels: standard contrast (signal,) and lo~ contrast (signal0. Ambient light at 1.3035 lux was measured and held constant for all subjects. A Schneider-Kreuznach carousel projector and Lafayette Tachistoscopic shutter were used to present the slides for 250 msec exposure at I sec intervals. At a focal distance of 65 cm, image size was 14×21 cm and stimulus size 6×5 cm. The slides were presented in 10 trials, 8 slides per trial, where p~,,,~, was 0.5 and invariant (4/8 slides were always blankl and P~g",q varied between 0.13 and 0.38. p,~,,~,, was held at 0.5 throughout all trials. Any trial contained standard stimuli with either matched (e.g., E. and Ej or F . and F0 or mismatched (e.g., E, and F~ or F , and Ej) low contrast stimuli. The subject was required to indicate detection by pressing a buzzer. Each trial was followed by a forced choice discrimination. The subject was asked to judge whether all the letters detected in that trial were the same, all E's or all F's, or a mixture of E's and F's. After trial 2, if the subject had not responded to any low contrast stimuli (SO a probe was delivered reminding the subject of his task. This process was repeated where necessary on trial 3, and then discontinued. Positive verbal reinforcement accompanied the subjects' first response to s~ and sjj regardless of trial. Auditory Continuous PeJ~brmance l e s t This consisted of a taped sequence of 5 phonemes of 144 sec duration. One phoneme was designated as relevant with a p of occurrence of 0.2 throughout the sequence. The number of events was 240 with an interstimulus interval of 0.20 sec and the number of relevant events 48 in toto. The subject indicated his detection of a relevant event by a buzzer press. RESULTS

Visual Information Processing Conditional probability m e a s u r e s (p~Dj/DII,) were calculated for the detection of low contrast stimuli (DO given the detection of normal contrast stimuli (DH). The forced choice discrimination data were converted to probability scores P~d, also. The product of these two scores (P(o, " P, DI/DII,) gives the visual attention score. A 3-way analysis of variance was performed on the data thus obtained and a significant F ratio was obtained for a main effect of Skin Reflectance, F(1,32)= 4.93, p<0.05), indicating a superior performance on the task by the low skin reflectance groups. The significance of the Skin Reflectance x Eye Color interaction, F(1,32)=4.45, p<0.05), indicated further that this superior performance was more marked in the subjects with light iris coloration. Measures of discriminability (Pos~) were obtained from the product of the detection scores (PD/D,) and the complement of the probability of false alarms (pf,,) thus: Pos~ =

PDI/DI[ " 1 -

Pra

The F ratio for Skin Reflectance x Iris Color was found to be significant, F(1,32)=4.85, p<0.05, indicating differential discriminability for the low contrast stimulus between the low skin reflectance groups; those with dark irides exhibiting a poorer performance on this measure. It should be noted that this measure did not produce a significant skin reflectance effect, which was observed in the visual attention scores.

257

a-MSH AND INFORMATION PROCESSING

[] Light Iris

• Female Dark Iris o Female Light Iris

•

Dark Iris

• Male Dark Iris ZXMale Light Iris

Visual Attention "9 . . . . . . . .

6

Discriminability

High reflectance

Low reflectance

5 []

.8-

4

.==3

o @@ o•

=2 '7-

y : .....

w. 6

l

I

I

I

2-4

7-9

2-4

7-9

Trials

Trials

= m m

FIG. 2. The shift of detection of low contrast stimuli from trials 2-4 to trials 7-9 demonstrates the selectivity of skin reflectance on the performance of the task.

"J

0

[]

-F

tion processing data. These measures were then subjected to 3-way analysis of variance. No significant effects were found.

I

I

High Low Skin reflectance FIG. 1. The interaction of skin reflectance and iris pigmentation on visual attention (Pd • Po~/oH) and discriminability (PDItDI l ' 1 -- Pta).

Figure 1 describes the two interactions found to be significant: Visual Attention (p~ • PD~/o~)and Discriminability (PDj/D. " 1 -- PrO. Finally, the scores were examined to determine any detection shift from early trials to later trials, providing a measure of pupilomotor and attentional activity. Trials 2-4 and 7-9 were selected for this comparison, as they were equivalent in terms of the number (6) of S~ presentations. Figure 2 summarises the grouped data obtained from the total scores of signalled detections of Sj in these sets of trials. A 4-way analysis of variance was used to examine these data and significant F ratios were obtained on the main effects of Iris Color, F(1,32)=7.21, p<0.05, and Trials, F(1,32)=55.01, p<0.01, indicating a greater facilitation for threshold in the performance between the two sets of trials for all groups.

Auditory Continuous Performance Test The data were converted from raw scores, NrespoaseJ48 to probability measures PrsR to conform to the visual informa-

DISCUSSION This study examined two aspects of previous behavioral findings on a - M S H activity, viz attention and threshold. Groups of children were selected for comparison (a) whose iris pigmentation was similar and whose skin reflectance measures were significantly different, and (b) others who differed in iris color but were similar in skin reflectance, with no notable difference due to sex in either group. The measure of skin reflectance is suggested as a developmental indicator of melanocyte presence, of melanin dispersion, and an index of t~-MSH activity. The data arising from the test of visual information processing was examined at three levels: (1) visual attention, encompassing the two-stage model of detection and discrimination; (2) discriminability, a simple measure o f stimulus detection including modification for response bias, and (3) a threshold over trials measure, all of which yielded significant effects, not always from the same source. The results for visual attention indicated a superior performance by groups with low skin reflectance, particularly those with light iris pigmentation, manifest in the significant interaction. These children perceived more of the low contrast stimuli, discriminated more effectively between stimulus types (E or F) and responded more correctly to the forced-choice questions. In as much as the groups with low skin reflectance may be deemed to have significantly more melanin presence due either to heavier investment of melanocytes or greater synthesis and dispersion activity, in particular those who by their light iris pigmentation may be presumed to have inherited a less dense type of melanin

258

FI~()YD AND KIN(i

deposition, their superior visual attention performance indicates a role for c~-MSH in the developmental mediation of this sensory activity. These findings therefore support the previous results of Sandman et al. [16,17] and the neurophysiological indicators manifest in the findings of Christensen et al. [2], and Goldman et al. [5]. Discriminability was seen to be significantly different only in the interaction described above. The group exhibiting facilitated performance consisted of the children with light iris pigmentation and low skin reflectance. This group perceived the low contrast stimuli with greater facility and consistency and with less deleterious response bias, in particular the girls, who gave no false alarms. While skin reflectance crossed with iris colour may have produced the interactions observed, it is nevertheless possible to attribute a degree of selectivity on the task to the main variable, skin reflectance. The skin reflectance measures in the low reflectance/light iris groups did not differ significantly from those in the low reflectance/dark iris groups. It is therefore less likely that many subjects from the latter group exhibited advanced-melanin pigmentation. Similarly, as low reflectance/light iris may be a more unusual combination, this group may have been more homogeneous than the other. It is evident, nevertheless, that the S~ discriminability varied over groups and that the input responsiveness of the light iris-low reflectance group was enhanced, consistent with those effects of MSH activity reported by Kastin et al. [8], Sandman e t a / . 1171 and the neurophysiological findings of Christensen et ,/.12], and Hanokoa 16]. The threshold over trials measure was examined to provide another perspective on the influence of this variable on the scores. The analysis of this measure yielded a significant effect over trials indicating improved performance by all groups as the test progressed and implicating to a limited degree the operation of pupillary adaptation. Further, a significant iris effect was noted with the facilitated performances arising from the lightly pigmented groups. Although compounded with attentional operations, the detection of stimuli by all light iris groups was superior by trials 7-9 to the dark iris groups, and in the light iris/low skin reflectance groups was superior at trials 2-4. The boys" performance in this group was better at trials 2-4 than all brown-eyed groups at trials 7-9. Since ambient light during these trials was held at 1.3035 lux and the order of presentation of the two tests was randomised, it is then possible to attribute the relative facilitation to pupillary or retinal operations or processes

directed towards improved acuity, e.g., Hanokoa I<)1repo, ts the activity of c~-MSH in the regeneration of rhodopsin and in the facilitation of light-dark adaptation The light iris, low skin reflectance group showed superiol visual information processing abilities. Together with the dark iris-low skin reflectance group, they detected and discriminated effectively at a significantly higher level of performance than groups with higher skin reflectance. The light iris-light skin reflectance groups who were equivalent to the superior group in detection of Sj by trials 7-9 were disadvantaged in other measures, their discrimination between stimulus letters and responses to the forced choice questions removing the advantage they may have gained in the detection. The question of the differential performance noted between the two iris color groups calls for further investigation. It is not generally accepted that iris color is an indicator of visual acuity or pupillomotor threshold. A u d i t o r y C o n t i n u o u s PerTfbrtnance 7 est,s

The analysis of these data revealed a homogeneity of performance over all groups. The test itself was applied in order to examine further aspects of attention. In consideration of the shift of sensory modality, it seems incautious to conclude yet that the presumed hormonal activity is confined to the visual systems. The auditory test does not encompass threshold measures, a variable which appeared to have significant activity in the previous test and which much of the literature seems to indicate as the main effect of MSH administration. A comparison of the means and standard deviations obtained for the two tests moreover, indicated a variation in difficulty for the population in question; the visual information processing test resulted in lower overall mean and greater standard deviation than the auditory test. In conclusion, the study demonstrated the concurrence of two events, previously documented to have occurred on administration of the hormone c~-MSH. Low skin reflectance coupled with light iris pigmentation was found to be significantly associated with enhanced visual information processing within the limits of a developmental continuum. The iris pigmentation was observed to affect threshold over trials significantly, an operation not sustained in attentional measures which indicated the greater influence of skin reflectance in the enhancement of visual attention.

REFERENCES 1. Bakay Pragay, E., A. F. Mirsky, B. C. Fullerton, H. Oshima and S. W. Arnold. Effect of electrical stimulation of the brain on visually controlled (attentive) behavior in Macaca Mulatta. Expl Neurol. 49: 203-220, 1975. 2. Christensen, C. W., C. T. Harston, A. J. Kastin, R. M. Kostrzewa and M. A. Spines. Investigations on a-MSH and MIF-I effects on cyclic AMP levels in rat brain. Pharmac. Biochem. Behav. 5: Suppl. 1, 117-120, 1976. 3. Fitzpatrick, T. B., M. Seiji and A. D. McGugan. Melanin pigmentation. New Engl. J. Med. 265: 328--332, 374--378and 430434, 1961. 4. Fitzpatrick, T. B., G. Szabo and R. E. Mitchell. Age changes in the human melanocyte system. In: Advances in the Biology o f the Skin, edited by W. Morgan. Oxford: Pergamon Press, 1964. 5. Goldman, H., E. B. Skelley, C. A. Sandman, A. J. Kastin and S. Murphy. Hormones and regional brain blood flow. Pharmac. Biochem. Behav. S: Suppl. 1, 165-169, 1976.

6. Hanokoa, K. Cited in C. H. Li. The chemistry of melanotropins. In: Hormona! Proteins and Peptides, edited by C. H. Li. New York: Academic Press, 1978. 7. Kastin, A. J., S. Jullander, N. E. Borglin, B. Dahlberg, K. Dyster-Aas, C. E. T. Krakan, D. H. Ingvar, M. Clinton Miller, C. Y. Bowers and A. V. Schally. Extra-pigmentary effects of melanocyte stimulating hormone in amenorrhoeic women. Lancet i: 1007-1010, 1968. 8. Kastin, A. J., L. H. Miller, D. Gonzalez-Barcena, W. D. Hawley, K. Dyster-Aas, A. V. Schally, M. L. V. Perra and M. Velasco. Psychophysiological correlates on MSH activity in man. Physiol. Behav. 7: 873-896, 1971. 9. Kastin, A. J., A. V. Schally, S. Viosca, L. Barrett and T. W. Redding. MSH activity in the pituitaries of rats exposed to constant illumination. Neuroendocrinology 2: 257-262, 1967.

a-MSH AND INFORMATION PROCESSING 10. Kaswan, J. and S. Young. Effects of luminance, exposure duration and task complexity on reaction time. J. exp. Psychol. 69: 393--400, 1965. 11. McGuiness, J., P. Correy and P. Proctor. Amorphons semiconductor switching in melanins. Science 183: 853-855, 1974. 12. Mirsky, A. F. and J. J. Tecce. The analysis of visual evoked potentials during spike and wave EEG activity. Epilepsia 9: 211-220, 1968. 13. Orzack, M. H. and C. Kornetsky. Attention dysfunction in chronic schizophrenia. Archs gen. Psychiat. 14: 323-326, 1966. 14. Panksepp, J., P. Reilly, P. Bishop, R. B. Meeker, T. R. Vilberg and A. J. Kastin. Effects ofa-MSH on motivation, vigilance and brain respiration. Pharmac. Biochem. Behav. 5: Suppl. 1, 59--64, 1976. 15. Rosvold, H. E., A. F. Mirsky, I. Sarason, E. D. Bransome and L. H, Beck. A continuous performance test of brain damage. J. consult. Psychol. 20: 343-350, 1956.

259 16. Sandman, C. A., J. M. George, T. R. MeCanne, J. D. Nolan, J. Kaswan and A. J. Kastin. MSH/ACTH4-1o influences behavioral and physiological measures of attention. J. din. Endocr. Metab. 44: 884--891, 1977. 17. Sandman, C. A., J. M. George, J. D. Nolan, H. Van Riezen and A. J. Kastin. Enhancement of attention in man with ACTH/ MSH 4--10. Physiol. Behav. 15: 427--431, 1975. 18. Sandman, C. A., J. George, B. B. Walker, J. D. Nolan and A. J. Kastin. Neuro-peptide MSH/ACTH 4-10 enhances attention in the mentally retarded. Phormac. Biochem. Behov. 5: Suppl. I, 23--28, 1976. 19. Sandman, C. A., W. D. Alexander and A. J. Kastin. Neuroendocrine influences on visual discrimination and reversal learning in the albino and hooded rat. Physiol. Behav. II: 613-617, 1973. 20. Sykes, D. H., V. I. Douglas and G. Morgenstern. Sustained attention in hyperactive children. J. Child Psychol. Psychiat. 14: 213-220, 1973. 21. Weatherhead, B. and A. Logan. Seasonal variations in the response of hair follicle melanocytes to melanocyte-stimulating hormone. J. Endocr. 81: 167, 1979.