Influence of lateral gaze on electroencephalographic spectral power

432

Electroencephalography and clinical Neurophy siology , 82 (1992) 432-437 © 1992 Elsevier Scientific Publishers Ireland, Ltd. 0013-4649/92/$05.00

EEG91529

Influence of lateral gaze on electroencephalographic spectral power B. De Toffol

a,b

A. Autret

a

B. Gaymard

a

and E. Degiovanni b

~Clinique Neurologique, and ~ Laboratoire d'Explorations Fonctionnelles Neurologiques, C.H.U. Bretonneau, 37044 Tours (France) (Accepted for publication: 5 October 1991)

Summary The effects of maintaining lateral gaze (as opposed to looking straight ahead) on electroencephalographic spectral power were tested in 12 right handed male subjects during eye opening (EO) and eye closure (EC). Our working hypothesis, based on Kinsbourne's paradigm, was that maintaining right lateral gaze activates the left hemisphere while maintaining left lateral gaze activates the right hemisphere, this activation resulting in a reduction in the spectral power over the hemisphere in question. Results showed that the variations in spectral power involved mainly the alpha frequency band. In the EC condition, the results were consistent with our working hypothesis: right lateral gaze produced a marked reduction in left hemispheric spectral power. In the EO condition, alpha power was constantly higher in the right hemisphere whether lateral gaze was maintained to the right or to the left. This can possibly be due to an attentional effect. Results are discussed with regard of the type of alpha rhythm and of the activation of cortical oculomotor centres. They shed light on the controversy concerning the existence of specific EEG correlates of cognitive activity, which preferentially involve each of the cerebral hemispheres.

Key words: EEG spectral power; Lateral gaze; Kinsbourne's paradigm; Alpha rhythm

By studying the gaze of subjects engaged in a cognitive task, Kinsbourne (1972) and Kinsbourne and Hiscock (1983) have shown that gaze position reflects the degree of involvement of each of the cerebral hemispheres in the task under study. Thus, activation of the right hemisphere produces preferential left lateral gaze, while activation of the left hemisphere results in preferential right lateral gaze. Neubauer et al. (1988) added EEG support to this theory by using the event-related desynchronization method and showed that left or right lateral movements correlated (under certain conditions) with the individual differences in the repartition of EEG spectral asymmetries. Later, a number of investigators (Gross et al. 1978; Honor6 1982; Lempert and Kinsbourne 1985; Honor6 et al. 1989)verified the inverse hypothesis: performance of a specific task, supposed to involve preferentially one of the cerebral hemispheres, is facilitated when gaze in maintained contralateral to the "active" hemisphere as opposed to staring straight ahead. The interest of this hypothesis is that it can be tested by using an EEG in an attempt to measure the possible activation of the hemisphere contralateral to the gaze deviation, independently of the cognitive activity. We used a recently developed method of signal treatment which allows the study of spectral asymmetries induced by cognitive activities which are

Correspondence to: Dr. 13. De Toffol, Clinique Neurologique, C.H.U. Bretonneau, 37044 Tours (France).

supposed to activate preferentially one of the cerebral hemispheres (De Toffol et al. 1990a). In general, preferential activation of one of the cerebral hemispheres is related to a reduction in the spectral power (SP) of the EEG activity over that hemisphere. The aim of our study was thus to analyse the effect of maintained lateral gaze on EEG spectral power with eyes opened and eyes closed. We attempted to test the hypothesis stating that maintaining right lateral gaze produces a reduction in left hemispheric spectral power while maintained left lateral gaze results in a reduction in the spectral power in the right hemisphere.

Subjects and methods Twelve young (20-25 years old) right handed (Oldfield's test 1971) males placed in a comfortable armchair in a softened light and a sound proofed room, underwent 6 sequences of testing, each lasting 2 min. Commands were communicated verbally between sessions. Three sequences were performed with the eyes closed (EC) and 3 with the eyes opened (EO): staring straight ahead (SSA-EC, SSA-EO), maintained right lateral gaze (RG-EC, RG-EO), maintained left lateral gaze (LG-EC, LG-EO). The SSA-EO sequence consisted in staring at a 3 cm diameter white paper circle which was easily seen, placed 1 m straight ahead of the subject and in the same horizontal plane as his eyes. The RG-EO and LG-EO sequences involved staring at

EFFECT OF LATERAL GAZE ON EEG SPECTRAL POWER

433

a circle located 45 ° to the right, or 45 ° to the left, respectively, in the same plane. This procedure did not produce extreme gaze deviations. Eye movements were verified by an electro-oculogram: one adhesive electrode was placed about 1 cm lateral to the outer canthus on each side. They allowed recording in a bipolar fashion, using a long time constant (0.7 sec). Right lateral gaze led to upward pen deflection while left lateral gaze led to downward pen deflection. Furthermore, during EO sequences, direct observation of the eye movements was made, through a little window, the subject being unaware of the observer's presence. Thus, the progression of each test was carefully controlled. All 6 sessions were arranged according to a latin square in order to eliminate any effect related to passing order. Six symmetrical derivations were recorded, with the reference placed on the vertex (Cz) in accordance with the American E E G Society guidelines (1991) C4-Cz, C3,Cz, C6-Cz, C5-Cz, P4-Cz, P3-Cz. The EEG was amplified by an Alvar polygraph (3 dB, 0.5 Hz-2.5 kHz). The spontaneous EEG activity was recorded on paper during the entire study in order to avoid artefacts. All of the subjects had a normal E E G with dominant alpha activity. Sampling was accomplished in real time at a frequency of 100 Hz using an analog-digital converter coupled to a MINC 11/23 and stored on a disk. Before sampling, the signal was filtered by anti-aliasing filters having a cut-off frequency of 30 Hz and an attenuation of 24 dB/octave. Processing was deferred. Successive elementary 2.56 sec spectra were calculated and each analysis period was filtered by temporal multiplication, using a Hanning window. Forty-eight elementary spectra were used to establish a definitive average spectrum. We considered spectra with a power greater than 200 txV2/Hz in the frequency band 0-1 Hz to be artifacts and consequently rejected them. Accordingly, 3 parameters were defined: SP (average spectral power in/xV2/Hz during a session), log SP, and the asymmetry index: AI = (SP r i g h t - S P left)/(SP right + SP left). The frequency bandwidths studied were: theta, 3.91-7.03 Hz; alpha, 7.03-12.89 Hz; betal, 12.89-19.92 Hz.

t test (df= 11). The log SP results are presented using untransformed power values (SP), but all significance analyses are based on log SP values.

Statistical analysis

O.10

We compared the different parameter values between sessions by a 1-way ANOVA of log SP and a 1-way ANOVA of AI (repeated measures of uni-dimensional variance analysis). We made 2 different comparisons (1) between EC sequences (SSA-EC, RGEC, LG-EC) and (2) between EO sequences (SSA-EO, RG-EO, LG-EO) in order to look for the existence of significant differences between staring straight ahead and lateral gaze sessions. When a significant difference was discovered ( P < 0.05), we compared each lateral gaze sequence and SSA sequence on the one hand, and the right lateral gaze to the left on the other hand, by a

Results

(1) Eyes closed tasks Study of the electro-oculogram showed that maintained right or left lateral gaze with eyes closed was associated with approximately one saccadic eye movement every 8-10 sec, in order ot maintain gaze lateralization. The subjects considered this task as difficult. (1.1) ANOVA log SP. Seven comparisons during 18 measurements (3 rhythms × 6 derivations) were significant. The spectral variations induced by lateral gaze involved the alpha frequency band in all derivations and the beta~ rhythm in C3-Cz. The results in the theta band were non-significant. The spectral power values for each gaze position (staring straight ahead, right gaze, left gaze) and each derivation are reported in the first line on Table I and in the upper portion of Fig. 1 for the alpha rhythm. Lateral gaze, either to the right or the left, induced a

Left hemisphere

Right hemisphere

PIJV2/Hz

15. ~ T

10.

SSA

-K-

"~

*

RG C6Cz

T

i

1I]

SSA

LG

RG CSCz

LG

A1

T 0.05

SSA

RG C6CzC5

LG

Fig. 1. Upper portion: spectral power (SP) values (/~VZ/Hz) of the eyes closed sequences for the alpha rhythm in C6-Cz (left part) and in C5-Cz (right part). SSA, staring straight ahead; RG, right gaze; LG, left gaze. *Significant t value ( P < 0.05) in the comparison between each lateral gaze sequence according to SSA. Lower portion: asymmetry index (AI) values of the eyes closed sequences for the alpha rhythm in C6-Cz-C5.

434

B. D E T O F F O L E T AL.

significant reduction in the spectral power over the two hemispheres as opposed to staring ahead in 11 out of 12 comparisons (t test). (1.2) ANOVA AI. Three comparisons during 9 measurements (3 rhythms × 3 pairs or derivations) were significant. The 3 significant comparisons involved the alpha frequency band. The results in both theta and beta I bands were non-significant. The AI values for each gaze position (SSA, RG, LG) are reported in the third line of Table I and in the lower part of Fig. 1. The AI, when staring straight ahead, was always positive (the spectral power was higher over the right hemisphere than over the left). Right lateral gaze produced a significantly higher index with respect to staring straight ahead 2 out of 3 times (t test). Left lateral gaze did not produce significant differences with respect to staring straight ahead. The t values obtained by comparison between right gaze and left gaze are: in C4-Cz-C3 t = 2.71 (P < 0.05), in C6-Cz-C5 t = 3.91 (P < 0.01) and in P4-Cz-P3 t = 2.62 (P < 0.05). Thus, the spectral power was always weaker over the left hemisphere during right gaze in comparison to left gaze (or spectral power was significantly weaker over the right hemisphere during left gaze in comparison to right gaze).

(2) Eyes opened tasks Staring at a paper circle seemed easy and was not considered tiring by the subjects. No saccadic eye movements were recorded by both electro-oculograms and direct observation during EO activities. (2.1) ANOVA log P. Two comparisons during 18 measurements (3 rhythms × 6 derivations) were significant: the first was for the alpha rhythm in C3-Cz and the second for the beta I rhythm in P3-Cz. The results in the theta band were non-significant. The spectral values for each gaze position in the C3-Cz derivation for the alpha rhythm are reported in the second line of Table I. Only spectral power during left gaze was significantly weaker in comparison to staring straight ahead (t test). (2.2) ANOVA AI. Three comparisons during 9 measurements (3 rhythms x 3 pairs of derivations) were significant: for the alpha rhythm in C3-Cz-C4 and in C5-Cz-C6 and for the beta~ rhythm in P3-Cz-P4. The results in the theta band were non-significant. The asymmetry index values for each gaze position (SSA, RG, LG) are reported in the fourth line of Table I for the alpha rhythm. During lateral gaze (right and left) the index values were significantly higher with respect to staring straight ahead (4 differences/4, t test). Thus,

TABLE I

Upper portion: spectral power (SP) values of alpha rhythm ( p N 2 / H z ) for derivations having a significant A N O V A difference for log SP in the eyes closed (EC) and eyes opened (EO) conditions, according to the gaze position. SSA, staring straight ahead; RG, right gaze, LG, left gaze. The t test values of the comparison between right gaze according to staring straight ahead are given in the R G column. The t values of the comparison between left gaze according to SSA are given in the LG column. Lower portion: asymmetry index (AI) values (alpha rhythm) for the derivation pairs having a significant A N O V A difference for AI in the EC and EO conditions, according to the gaze position. The t values of the S S A / R G comparisons are given in the R G column and S S A / L G comparisons in the LG column. C4-Cz

C3-Cz

SSA R G

LG

SSA R G

C6-Cz LG

SSA R G

C5-Cz LG

SSA R G

P4-Cz LG

P3-Cz

SSA R G

LG

SSA

RG

LG

ANOVA log P

EC SP t

6.76 5.94 5.19 6.16 4.49 4.33 15.8 14.51 13.10 14.35 10.99 11.15 37.48 31.04 27.06 29.57 23.05 22.64 2.22 * 3.10 * 4.33 * 4.24 * 2.57 * 2.67 * 4.38 ** 2.96 * 3.78 * 3.10 * 3.16 * 2.17

EO

sP

3.98 3.92 0.52

t

3.28 2.30 *

C4-Cz-C3 SSA

C6-Cz-C5

P4-Cz-P3

RG

LG

SSA

RG

LG

SSA

RG

LG

0.13 -2.9 *

0.04 -1.21

0.06

0.14 -2.86 *

0.07 -0.31

0.10

0.14 -1.52

0.07 1.74

0.05 - 3.22 * *

0.07 - 2.92 *

0.00

0.04 - 2.48 *

0.08 - 3.02 * *

ANOVA A I EC AI t

0.03

EO

sP t

- 0.02

* t value significance ( P < 0.05); * * P < 0.01.

EFFECT OF LATERALGAZE ON EEG SPECTRALPOWER the spectral power was always higher in the right hemisphere during both right and left gaze in comparison to staring straight ahead.

Discussion

Our hypothesis, based on Kinsbourne's work, is that maintained right lateral gaze may "activate" the left hemisphere in comparison to staring straight ahead while maintained left lateral gaze may "activate" the right hemisphere. Such an "activation" is manifested by a reduction in spectral power in the EEG. In the eyes closed condition, maintained right or left lateral gaze produced a reduction in alpha power over the two hemispheres as compared to staring straight ahead. In accordance with our hypothesis, right gaze is clearly related to activation of the left hemisphere. Activation of the right hemisphere by left gaze is less obvious and can only be documented by left gaze/right gaze comparisons. In the eyes opened condition, maintained right or left lateral gaze only produces a reduction in alpha power in the C3-Cz derivation in comparison with staring straight ahead. During both right and left gaze, the spectral power is higher over the right hemisphere as compared to staring straight ahead in the central derivations. Thus, our hypothesis is not verified in the eye opened condition. The general method of signal analysis, the parameters tested and the statistical method used have been discussed in an earlier publication (De Toffol et al. 1990a). However, both montage choice and electrode location require further explanations. A referencevertex montage (Cz) may record unpredictably and unequally from either or both hemispheres since Cz is not a neutral reference. Nevertheless, to demonstrate EEG asymmetries, such a montage is preferable (see review in Beaumont 1983). In our previous work (De Toffol et al. 1990a) we simultaneously used 3 different derivations: bipolar, reference-vertex and ear-linked (EL) (i.e., C5-P3/C6-P4, C5-Cz/C6-Cz C5-EL/C6-EL) to record LEG activity during both sensorimotor and neuropsychological tasks. Both SP and asymmetry index values were calculated. Our conclusions were as follows: (1) the asymmetries recorded did not change whatever the montage; (2) the Cz derivation detected the greater number of LEG asymmetries according to the parameters used. The centro-parietal electrode location is consistent with the aim to record "activation" of one hemisphere. The alpha frequency band studied does not correspond to the classical occipital rhythm which blocks with eye opening. It is related to the cognitive processes which preferentially involve the centro-parietal regions (see below) (Galin et al. 1982; De Toffol and Autret 1991).

435 In order to discuss our results and to suggest an explanation for the differences found between the eyes closed and eyes opened conditions, we have to consider the origin of the alpha activity during the eyes closed condition in relation with lateral gaze. Alpha desynchronization globally reflects an activated state in large cortico-thalamic regions and indicates a diffuse excitability state (Steriade et al. 1990). In primates, eye movement direction is controlled by the cortex of the frontal lobes (Bruce and Goldberg 1985). A positron emission tomographic (PET) study showed that saccadic eye movements are associated with rCBF increase within the frontal eye fields and the supplementary motor areas of both hemispheres (Fox et al. 1985). An important neuronal network implicated in motor orientation in relation with cognitive functions has been demonstrated by Gur et al. (1983), using PET. Thus, lateral gaze can largely activate the hemispheres, especially when one considers the large number of repeated saccadic eye movements found in the electro-oculogram, which are related to the periodic activation of cortical neuronal networks. The reduction in spectral power which is seen over the two hemispheres during right and left gaze is encountered during the course of various activities, whether purely sensorimotor, purely neuropsychologic or both neuropsychologic and motor (Gevins et al. 1980; Olivan et al. 1984; Autret et al. 1985; De Toffol et al. 1990a; De Toffol and Autret 1991). This is a non-specific effect related to the activity itself, independent of any specific cognitive contents. CBF studies have shown that, whatever the type of mental or sensorimotor activities considered, both hemispheres are involved (Maximilian 1982; Fox et al. 1985; Deutsch et al. 1986; Papanicolaou et al. 1987). The CBF is a reflection of local neuronal metabolic activity (Raichle et al. 1976; Yarowsky and Ingvar 1981) and there is a correlation between the CBF and EEG activity (Ingvar et al. 1976). Maintained lateral gaze in right-handed subjects, however, does not equally activate each of the contralateral cerebral hemispheres: right gaze clearly activates the left hemisphere while left gaze has less of an effect on the right hemisphere. Warren and Haueter (1981) reported that a substantial contributor to the production of task-related alpha asymmetries is the direction of spontaneous lateral eye movements which co-occur with cognitive activity. Right-looking induced a more pronounced alpha attenuation in the left hemisphere than left-looking did in the right hemisphere. Asymmetry of response to lateral gaze suggests that contralateral attenuation of alpha activity by eye deviation is not related simply to the projection of each hemifield to the contralateral hemisphere, but reflects some more specific effect related to localization of function. It may be significant that contralateral alpha

436

attenuation is more evident in the left hemisphere, which also shows a greater degree of specialization of neuropsychological functions (Bryden 1982). The activating effect of lateral gaze seen in the EEG during rest is also demonstrated when one of the hemispheres is preferentially involved in a cognitive activity. We recently studied the effects of lateral gaze on EEG spectral power in a subject whose left hemisphere had been previously "activated" by performing a memorized writing task with the right hand with eyes closed. In this situation, left hemispheric activation, as measured by the increase in the asymmetry index during staring straight ahead, was removed by maintaining left lateral gaze (De Toffol et al. 1990b). Thus, one should clearly distinguish: (1) gaze movements during cognitive activities which are related to asymmetric activation of the cerebral hemispheres, corresponding to Kinsbourne's classic paradigm (Kinsbourne 1972; Warren and Haueter 1981; Neubauer et al, 1988); (2) the increase in performance of a task which supposedly preferentially activates one hemisphere through maintained contralateral gaze as opposed to staring straight ahead and corresponding to Kinsbourne's inverse paradigm (Gross et al. 1978; Honord 1982; Lempert and Kinsbourne 1985; Honord et al. 1989); (3) the direct effect of maintained lateral gaze on the activation of each of the hemispheres as measured by the EEG independent of any cognitive activity and which is the subject of this present study. These 3 distinct aspects illustrate the concept of functional specialization in the cerebral hemispheres. Our findings are consistent with the comprehensive model of psychophysiological functions according to lateralization which implies a lateralized co-occurrence of cognitive activity, attention, eye movements and alpha activity (Ulrich 1990). In the eyes opened condition, the alpha power is less influenced by the gaze position than in the eyes closed condition. This finding can be explained by 2 reasons: firstly, by the fact that maintained lateral gaze is characterized by alpha desynchronization and the power of this rhythm is considerably reduced during eye opening as opposed to eye closure (Adrian and Matthews 1934). Secondly, by the disappearance of saccadic eye movements related to fixed gaze and thus lower activation of the frontal oculomotor neuronal networks. Using a different method, we have already demonstrated the effect of lateral gaze with the eyes opened on the repartition of resting spectral asymmetries (Autret et al. 1985). Our study cannot be compared to the Mulholland and Evans's work. These authors found large increases in the amplitude of occipital alpha rhythm upon looking upwards with eyes opened (Mulholland and Evans 1965) or during extreme left or right downward deviation, conditions which are incompatible with fixation (Mulholland 1969).

B. DE TOFFOL ET AL.

The variations in the asymmetry index show that, whatever the gaze direction, power is always higher over the right hemisphere. Our initial hypothesis is no longer verified. This relative increase in alpha power in the right hemisphere may be explained by an attentional mechanism related to eye opening. Indeed, Ray and Cole (1985) showed that the attention aspect of a cognitive task was related to the variations in average power (from 8 to 15 Hz), including the alpha rhythm. In subjects performing "internal"cognitive tasks (socalled "rejection tasks") the alpha power is significantly higher over the right hemisphere than during tasks which imply an analysis of environmental factors (so-called "intake tasks"). Thus, maintaining lateral gaze, outside of all cognitive activity, asymmetrically modifies the alpha frequency band in comparison to staring straight ahead. In the eyes closed condition, the demonstrated variations (especially the capacity of right gaze to activate strongly the left hemisphere) offer EEG support to Kinsbourne's paradigm. In the eyes opened condition, the superposition of attentional factors produces a relative increase in alpha power over the right hemisphere irrespective of the gaze position. These results are helpful for discussing the contradictory studies concerning the relationship between the EEG and cognitive activities (Gevins and Schaffer 1980). Two main conclusions arise: (1) the necessity of controlling eye movement direction during cognitive tasks; (2) the importance of distinguishing cognitive tasks accomplished in the eyes closed condition from those which take place with the eyes open and when specific EEG patterns, perhaps related to attentional factors, intervene. We thank Dr. Donald Schwartz and Dr. Richard Desbiens for their help in the translation of the manuscript.

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