The laterality of photic driving in normal adults

290

ELECTROENCEPHALOGRAPHYAND CLINICALNEUROPHYSIOLOGY THE

LATERALITY IN

OF

NORMAL

PHOTIC ADULTS

DRIVING 1

ROBERT W . LANSING AND HARRY THOMAS 2

Department o f Psychology, UniversiO, o f Arizona, Tucson, Ariz. (U.S.A.) (Received for publication: August 27, 1962) (Resubmitted: April 19, 1963)

Although photic drivinga asymmetry has been studied frequently in neurological patients, the laterality of driving in normals has received comparatively little attention. Marked asymmetries (hemispheric differences in amplitude of 50°0 or greater) apparently occur in about 5 per cent of the normal population (Kooi et al.

dominant hemisphere. The effects of monocular stimulation on driving laterality have not been studied in man; in the monkey, flickering light presented to one eye produces the greatest driving over the contralateral hemisphere (Walker et al. 1944). Selectively stimulating the right or left visual field, Adrian (1943) observed that only

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the hemisphere contralateral to the flickering half-field was driven. In a similar experiment however, Toman (1941) reported that stimulating only half of the visual field produced driving over both hemispheres. In the present investigation, the laterality of photic driving in normal subjects was studied during binocular, monocular and half-field stimulation, with flash frequencies above, within, and below the alpha range. METHOD Thirty-four normal adults (ages 17 to 38, 10 female and 24 male) served as subjects in the two experiments

Electroenceph. clin. NeurophysioL, 1964, 16:290-294

291

LATERALITY OF PHOTIC DRIVING described below. E E G s were recorded scalp to scalp from the right, left, and midline occipital parietal regions, with a six-channel Grass Model 5 Polygraph (with EEG preamplifiers). Using a plastic template to assure homologous placements, electrodes were placed as follows: occipital leads 1 cm above the inion on the midline, and 4 cm laterally to the left and right of midline; parietal leads 8 cm above the occipital leads on the midline, and 5.5 cm to the left and right of midline. In the first experiment, the laterality of photic driving during monocular and binocular stimulation at low (4 to 6/sec), medium (8 to 12/sec) and high (16 to 20/sec) flash rates, was studied in each of 29 subjects. The experimental plan and apparatus are outlined in Fig. 1. Subjects viewed the stimulus fields (S) stereoscopically, fixating points (on transparent sheet F) in the center of each stimulus field. Identical flashes were delivered to each eye with Sylvania R1131C Glow Modulator tubes (G) controlled by two Grass S 4 stimulators: these were operated independently for monocular stimulation and synchronously for binocular stimulation. The 150 V output of the stimulators fired the glow tubes through a trigger circuit which produced 250 V, 55 mA square pulses. The flickering light field subtended a visual angle of 54" horizontally and 3 5 vertically for each eye; the stimulus flashes were of 333 ft-c intensity, 10 msec in duration, and were delivered in 20 sec bursts. To assure the delivery of equal flash intensities to each eye, photocell (P) responses were recorded continually on the inkwriter and periodically with a CRO. Presentation of the several stimulation frequencies and modes was systematically varied to avoid order effects. In a second experiment, the laterality of driving during full-field, and left and right half-field stimulation was studied ineight subjects. E E G s w e r e r e c o r d e d a s a b o v e , but stimuli were presented with a Grass PS 2 photostimulator (intensity setting 8) transilluminating an opal glass strip (visual angle 34 '~) between two dark areas. The subject fixated the left margin of the lighted strip for right-field, the right margin for left-field, and the center for fullfield stimulation. Handedness (the hand normally used for writing) was determined for all subjects although this was incidental to the main purpose of the study.

RESULTS AND DISCUSSION The laterality of photic driving was determined by making wave-to-wave comparisons of driving potentials recorded from the left and right occipital-parietal areas. The criterion of laterality was an average amplitude difference of 10 per cent or greater between the two hemispheres: each subject was categorized as left-dominant, right-dominant, or symmetrical under each experimental condition. For some subjects, driving responses were not clear enough to be analyzed, particularly with monocular stimulation at high or low frequencies. The laterality of the resting (eyes closed) alpha rhythm was determined according to the method just described for photic driving.

Experiment 1: Binocular and monocular stimulation at high, medium and low [tash rates The results, summarized in Table 1, show that only a few subjects had symmetrical driving responses; for most subjects, driving was greater over the left hemisphere regardless of the mode or frequency of stimulation. In five (17% of the group) the difference in driving amplitude between the two hemispheres was greater than 50 per cent. The consistency of lateralization for individual subjects was the most striking finding in this experiment. Of seventeen subjects with measurable driving responses to binocular and monocular stimulation (at medium flash rates), fifteen showed the same laterality whether or not the left eye, right eye or both eyes were stimulated. When eleven subjects with clear driving for all flash rates and modes of stimulation were considered, eight were completely consistent showing the same laterality under all conditions. These findings were statistically significant (P <0.001) when tested by the Z2 method. Recordings from a single subject (Fig. 2, 3) illustrate the constancy of lateralization found in this group. The three individuals who failed to show complete uniformity of response had either left dominant or symmetrical driving for most conditions of presentation. Nearly all of our subjects were right-handed, with the alpha rhythm and photic driving lateralized to the left hemisphere (Table I). A relationship between handedness and EEG laterality is difficult to establish on the basis of these results since handedness, itself, was determined in a

TABLE I N u m b e r of subjects, of a group of 29, showing left-dominant, right-dominant, or symmetrical driving under different conditions of stimulation. Handedness, and laterality of the occipital alpha rhythm are also shown

Laterality Left Right Symmetrical N o measure

Binocular

Left eye

Right eye

Alpha

Med. Low High

Med. Low High

Med. Low High

rhythm

18 4 0 7

11 4 3 11

18 1 1 9

11 4 2 12

9 3 3 14

14 1 2 12

13 3 2 11

11 2 4 12

14 2 2 11

18 5 3 3

Handedness

5 24 -0

Electroenceph. clin. Neurophysiol., 1964, 16:290-294

R. W. LANSING AND H. THOMAS

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Fig. 2 Occipital-parietal recordings from subject S. G. showing the laterality of photic driving at different flash frequencies during binocular stimulation. (See Fig. 3 for explanations.) rather approximate way and since, of the five left-handed subjects studied, only one had right dominant alpha or driving responses. Our results differ from those of Cornil and Gastaut (1951) who found that the alpha rhythm and photically evoked responses were lower in amplitude over the dominant hemisphere. Raney (1939), Strauss et al. (1943) and others found a lower alpha amplitude over the dominant hemisphere while Williams and Reynell (1945) and Glanville and Antonitis (1955) failed to find any relationship between alpha symmetry and lateral dominance. We do not know how to account for these divergent results; they may be related to the lack of uniform criteria for determining lateral dominance (see Benton 1962) or perhaps to variations in scalp derivations, if there are regional differences in alpha symmetry (see Raney 1939).

Experiment 2: Full-field, and right and left half-field stimulation Eight subjects were studied in this experiment, four with greater driving over the left hemisphere and four with greater driving over the right during full-field stimu-

lation. As shown in Table II, restricting the flickering light to the left or right visual field did not change the laterality TABLE l l Laterality of photic driving with full field, left field, and right field stimulation Subject R.H. H.M. G.S. A.C. M.B. Z.D. R.L. G.E.

Full field R R R R L L L L

(13) (20) (2) (10) (44) (21) (18) (4)

Left field R R R R L L L R

(5) (7) (15) (12) (22) (10) (13) (45)

Right field R R R R L L L L

(10) (14) (24) (l) (31) (24) 07) (22)

L: greater driving over left hemisphere. R : greater driving over right hemisphere. ( ): Percentage difference in amplitude between the two hemispheres.

Electroenceph. clin. Neurophysiol., 1964, 16:290 294

293

LATERALITY OF PHOTIC DRIVING

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Fig. 3 Recordings from the same subject during monocular and binocular stimulation at 11 flashes per sec. PC : photocell response; LOP: left occipital-parietal; ROP: right occipital-parietal; MOP: midline occipital-parietal. of the driving response for most subjects (this effect was statistically significant by Zz test, P <0.001). The degree of laterality, expressed as the percent amplitude difference between the two hemispheres, did not change in any consistent fashion. The one subject, G.E., who showed a reversal of laterality as the field of stimulation was changed also displayed a shifting asymmetry with full-field stimulation. Adrian (1943) reported that driving could be readily reversed by changing the visual half-field stimulated. Since, in his experiment, driving appeared only over the hemisphere contralateral to the field of stimulation, he concluded that the localization of driving potentials was in agreement with the cortical projection of the optic pathways. We found, however, in agreement with Toman 0941), that driving responses were produced bilaterally with half-field stimulation, and were in fact often of greater amplitude over the hemisphere ipsilateral to the field of stimulation. Gastaut (1949), recording flicker potentials directly from the subcortex of the occipital

lobe, observed that the topography of the driving response was not altered by changing the field of stimulation. We conclude, therefore, that driving potentials must be elaborated largely through bilateral projections to the occipital cortex from subcortical centers, or through interhemispheric connections beyond the striate area. The difference between our results and those of Adrian may lie in the fact that for a few individuals driving laterality is determined by the field of stimulation. On the basis of our two experiments, we suggest that the laterality of photic driving in normals is determined by intrinsic cerebral factors rather than asymmetries in the activity of the direct visual paths to the cortex. These "intrinsic factors" might include hemispheric differences in the situation or number of cortical neurons giving rise to the rhythmic response, or asymmetries in the functioning of subcortical systems involved in the regulation of cortical driving (although such systems have not to our knowledge been identified). The asymmetries which persisted in our subjects in spite of changes in the mode

Electroenceph. clin. Neurophysiol., 1964, 16:290-294

294

R. W. LANSING AND H. THOMAS

or frequency of visual input are not attributable to inequalities of registration from the two hemispheres since the electrodes were carefully positioned bilaterally, and the LEG channels were occasionally reversed to record from opposite hemispheres. Our experimental group is too small to serve as a normal base against which to evaluate asymmetries in neurological patients. It seems clear that hemispheric differences in driving amplitude resulting from a lateralized organic disturbance will be superimposed on a normal asymmetry, varying in degree from person to person. The effect of cerebral dysfunction on driving symmetry may therefore either be attenuated or enhanced depending on the pre-existing laterality of the normal response. There is an additional application of these resuits to the study of both normal and patient groups. Photic driving asymmetries cannot readily be accounted for by faulty positioning of the stimulus source, ocular defects, or any other condition influencing only the direct visual input to the cortex over classical projection paths. Gross manipulation of this input may reduce the amplitude or persistence of driving, but, as shown her ,~ rar~.ly effects the laterality of response. SUMMARY The laterality of photic driving was determined for 34 normal adults, analyzing recordings from the left and right occipital-parietal regions. The majority of subjects were right-handed and showed left-dominant driving responses. Driving laterality was independent of the mode (binocular or monocular), frequency, or field of stimulation, and was highly consistent for any given individual. These results are interpreted asc&owing the importance of intrinsic cerebral factors in determining the laterah / of photic driving in normal man. REFERENCES ADRIAN, E. D. Doyne memorial lecture; dominance of vision. Trans. Ophthal. Soc. U. K., 1943, 63: 194-207. BENTON, A. L. Clinical symptomatology in right and left hemisphere lesions. In V. B. MOUNTCASTLE (Editor),

Interhemispheric relations and cerebral dominance. Johns Hopkins, Baltimore, 1962: 253-264. BRAZIER, M. A. B., COB8, W. A., FISCHGOLD, H., GASTAUT, H., GLOOR, P., HESS, R., JASPER, H. H., LOEB, W., MAGNUS, O., PAMPIGLIONE, G., RI~MOND, A., STORM VAN LEEUWEN,W. and WALTER,W. GREY. Proposal for an LEG terminology by the terminology committee of the International Federation for Electroencephalography and Clinical Neurophysiology. Electroenceph. clin. Neurophysiol., 1961, 13: 646-650. CORNIL, L. et GASTAUT, H. Note complementaire sur l'Gtude 61ectroencGphalographique de la dominance cGrGbrale (b, propos de la gaucherie). Ext. C. R. Congrds des Mddecins Alidnistes et Neurologistes, 16-23 juiUet, 1951. GASTAUT, H. Enregistrement sous-cortical de l'activit6 61ectrique spontanGe et provoquGe du lobe occipital humain. Electroenceph. clin. Neurophysiol., 1949, 1: 205-221. GLANVILLE, A. D. and ANTONITIS, J. J. The relationship between occipital alpha activity and laterality. J. exp. Psychol., 1955, 49: 294-299. HUGHES, J. R. and CURTIN, M. J. Usefulness of photic stimulation in routine clinical electroencephalography. Neurology (Minneap.), 1960, 10: 777-782. KOOI, K. A., ECKMAN, H. G. and THOMAS, M. H. Observations on the response to photic stimulation in organic cerebral dysfunction. E/ectroenceph. din. Neurophysiol., 1957, 9: 239-250. RANEY, E. T. Brain potentials and lateral dominance in identical twins. J. exp. Psychol., 1939, 24: 21-39. STRAUSS, H., LIBERSON, W. T. and MELTZER, T, Electroencephalographic studies: bilateral differences in alpha activity in cases with and without cerebral pathology. J. Mr. Sinai Hosp., 1943, 9: 957-962. TOMAN, J. Flicker potentials and the alpha rhythm in man. J. Neurophysiol., 1941, 4: 51-61. WALKER, A. E., WOOLF, J. l., HALSTEAD, W. C. and CASE, T. J. Photic driving. Arch. Neurol. Psyehiat. (Chic.), 1944, 52: 117-125. WILLIAMS, D. and REVNELL, J. Abnormal suppression of cortical frequencies. Brain, 1945, 68: 123-161.

Reference: LANSING, R. W. and THOMAS, H. The laterality of photic driving in normal adults. Electroenceph. clin. Neurophysiol., 1964, 16: 290-294.