- Email: [email protected]
Is there an interaction between cognitive activity and lateral eye movements?
Neurolnyc.holosit, Vol. 18, pp. 591 to .596 :~ Pe~-~OmonPress Ltd., 1980. Priated in Gnmt Britain
0028-3932/80/1001--0591 $02.00/0
NOTE IS THERE AN INTERACTION BETWEEN COGNITIVE ACTIVITY A N D LATERAL EYE MOVEMENTS? WOLFGANG S~UNG and DETLEV VON C~,AMON
Abteilung ffir experimentefle Nenrologie, Max-Planck-Institut fur Psychiatric, D-8000 Mfinchen 40, Kraepelinstra~ I0 (Received 11 February 1980) Almraet--recording lateral eye movements of Ss with eyes opened in a dark room, no influence of the task on the first eye movement following the question could be detected. An analysis of all eye movements showed a directional preponderance to the left at certain parts of the verbal tasks.
SINCE the first works of'rgd'rEt.gAUMEli and DAY [2], the relationship of lateral eye movements following a question to information processing ['l, 3, 4], several individual differences and, more importantly, to cerebral lateralisation have been the subject of a great number of publications (for references see the review of Em~ICt[MA~ and W~OU, [5]. However, the two main problems arising from these articles have been the hypothesized relationship between hemispheric asymmetry and the direction of eye movements, and the diffgulties involved with the qmmtions and methods used for examination. A theory concerning the intera~ion between cerebral activation and a deviation of Ilaze directed contralaterally to the "active" hemisphere was first proposed by BAKAN [6]. He thought that as eye movements were controlled contralaterally by activity in the "frontal eye field" (Brodman area 8), the left- or right-movement could be "symptomatic of easier triggering of activities in the hemisphere contralateral to the direction of eye movement". KINSDOURNE[7] modified this model He proposed that as "the cerebrum is a highly linked system", verbal activation could overflow into the left-sided orientation center, "driving attentional balance off center and to the right". Recent papers have seldom tried to reconsider these theories in the light of new neuroanatomical mad neurophysiological findings. These findings showed that area 8 does not specifically control the direction of eye movements [8, 9, I0]. The model of Kinsbournc of an "overflow" of activation to an "orienting center" likewise seems much too simplified [ 11"]. "How the central nervous system generates saccades is still speculative" (RAPHAN and CottoN, 1"12]). As Etmt.iCnMAN and Wu~mJmou [5] recently offered a very detailed analysis of the theoretical research concerning "lateral eye movements" and of the methodological problems involved, we confine ourselves to a short comprehensive summary of their work. The main difficulties are: (a) the situation: to what extent does the field of vision, the localisation of the experimenter, and the acoustical background influence the direction of eye movements? (b) the recording and g o r i n g of the eye movements: which movements are to be recorded, and which method of recording should be used? Should stares and vertical eye movements be included? (c) the kind of the questions asked; do they mainly activate only one hemisphere? In accordance with EHm.ICM~N and W m m m ~ c ~ [5], we started from the consideration that there is no reason to presume that the influence of a question would result only in a deviation of the first eye movement. If all environmental factors that could lead to a directional shift are (as far as possible) excluded, then any influence should be detectable.
METHODS Subjects Thirty persons (18 women, 12 men) between 16 and 30 years ofage served as subjects. Their handednes$ was tested by eight different tasks [13]; 27 persons were right-handed, 2 left-handed and 1 person left-handed as a child was now right-handed. The subjects were told that the experiment was to measure their ability to concentrate in darkness, and that an EEG would be recorded. 591
592
NOTE
Materials Three kinds of questions were used: 30 verbal questions [the Ss had to build a sentence of two words (randomlypaired German words, containing one or two syllables)]; 30 arithmetical questions (multiplication of a one-digit number by a two-digit number between 10 and 20); and 30 musical questions (Ss had to hum four tones in imitation of a flute).
Situation During the experiment, Ss lay on a bed in a room 3.5 m x 2.5 m x 2.2 m. The room was completely dark (confirmed by all Ss). Their head was fixed in a normal position, so as to avoid a superpmition of eye and head movements. The Ss were instructed to keep their eyes open during the whole semion (this was supervised by the experimenter). The soundproof room was screened from possible electrical disturbances, the only sound continuously heard was the buzzing of an air-conditioner keeping temperature and atmospheric moisture constant. The questions were presented from a tape-recorder through a loudspeaker located directly behind the S's head. The responses of the Ss were transmitted to the experimenter outside the room by means of a microphone.
Desujn of the experiment Each question was divided into five parts: an interval it (before the question), interval i2 (question), interval i3 (the S "solves" the problem), interval i4 (answer) and interval i5 (fixed interval after the answer). Figure I shows this. The beginning of each interval was recorded by the experimenter who gave different trigger signals to the computer being used (PDP 11/40). The experiment began with five minutes of a first baseline (Ss were instructed to lie silently), then came the first block of 45 questions, randomly divided into 15 verbal, 15 arithmetical and 15 musical questions. Then came another baseline, then the second block with again 45 questions, and then the third baseline. Each baseline took 5 minutes; each block about 15 minutes. The beginning and the end of each block and each baseline were also recorded.
Subject is awaiting the quest ion
,
~
listening to the question
,,
~'N
answering
thinking
,,
A
"
~
'
i,,
sa
I
i ,, i
fixed inter-about 3 vai a f t e r sec untJ[ the end of the next the ,~nsww question
Fro. 1. Temporal soquence of a question.
Apparozus and recording The eye movements of the Ss were recorded continuously by an electrooculogramm (EOG). Four channels (each eye was monitored horizontally and vertically) were A-C recorded (time constant 5 seconds) on a Beckman Dynograph, using s/lvet,-e/Iver chloride electrodes (skin resistance below 5 k~). The recorded signals were given to the computer, which was programmed to identify sazcadic eye movements [14]. Only saccades with an amplitude of more than 5° and with a maximum angular velocity of more than 180°/sec were scored, thus excluding "noise" and slow dril~ movements from the analysis. With the help of the trigger signals indicating the relevant points of time, the eye movements of the Ss could be calculated for each interval.
Scormo of the eye movements We limited our analysis to the horizontal s~_cc~_des,or the horizontal components of vertical and oblique saccades. The way of recording used in this experiment did not register a constant zero-line, i.e. the ~ . d i r e c t i o n "straight on" could not be defined unequivocally; in addition, saccades from different starting-points are only comparable to a limited degree. Therefore, we only scored eye-movements going to the right or to the left in relation to their previous position.
24.7 12.6 25.9 16.6 21.9 30.3 30.9
il i2 i3 i4 i5 i2-4 i3-4
22.2 13.0 33.4 20.7 14.9 41.4 38.7
% Left 53.1 74.4 40.7 62.8 63.1 28.2 30.4
184 177 168 157 129 141 157
Verbal questions % None t W
ns ns ns us 5% ns ns
P 26.8 11.2 21.2 6.7 17.6 28.4 23.4
% Right 24.7 14.3 20.3 8.0 15.2 28.4 24.7
48.6 74.4 58.4 85.3 67.2 43.1 51.9
212 209 231 208 184 225 214
Arithmetical questions % % Left None t W
ns ns ns ns ns ns ns
P
8.1 5.4 9.1 8.7 9.5 8.3 9.2
8.3 5.3 10.8 10.3 7.2 9.4 10.7
210 193 160 151 134 122 117
Verbal questions Frequency of saecades Right Left t W
ns ns ns ns 5% 5% 2%
p 9.6 5.2 7.2 8.1 8.9 6.3 7.1
8.9 6.0 7.8 8.1 7.3 7.0 7.7
177 193 193 160 165 171 193
Arithmetical questions Frequency of saccades W Right Left t
Freque~y of saccades: values calculated per minute; Right, Left: saccades to the right or the left. W: Wilcoxon Test (see Table 1). il-i5: the intervals of each question (see Fig. 1).
il i2 i3 i4 i5 i2--4 i3-4
Intervals
ns ns ns ns ns ns ns
p
Table 2. Directional preponderance of saccades of each interval
% Right, ~o Left: percentage of lateral eye movements to the right and to the left. % None: percentage of intervals where no saccade was made. W: result of the Wilcoxon Test, t: t-values, p: level of significance (as: not significant, 5%: significance of 5 %l il-5: the intervals of each question (see Fig. 1).
% Right
Intervals
Table 1. Direction of the first lateral eye movement of each interval
29.4
21.8 14.2 22.3 19.1 20.7 35.7
% 51.1 72.6 65.2 59.0 57.8 37.1 43.0
None
8.8 4.7 9.1 10.1 10.4 7.5 9.8
7.6 4.9 13.4 9.5 9.2 8.3 10.8
143 214 149 205 191 188 189
Musical questions Frequency of saccades Right Left t
27.1 13.2 12.4 21.9 21.6 27.2 27.5
Left
Right
Musical questions
%
%
W
209
161 198 138 205 218 178
t
w
ns ns ns ns us ns ns
p
ns
ns ns ns ns ns us
UJ
Z
594
NOTE
RESULTS Direction of the.~rst saccade of each interval For each interval of the question, we tested whether a ~__~__dehad been made, and in which direction the first saccade occurred. In order to have data comparable to those presented in the studies concerning lateral eye movements, we alao tested the combined intervals D-it and i2-i4. The combined interval i3-it represents the first eye movement following the end of the question, and the combined interval i2-it, the first eye movement following the beginning of the question (a value also scored in some papers). Table 1 gives the percentage values of'first __~,~_ _~es" in each interval directed to the right or to the left, and the proportion ofintervala without eye movements. In order to obtain the diffegencm of these values, the Wilcoxon Test was calculated over the mean values of each person (i.e. each value represented the mean of the 30 questions of each kind the Ss were asked). During the relevant intervals i2, i3, it, no significant differences appeared. Additionally, we calculated the differences for the individual data for the combined interval i3-it by means of the Binominai Test. On a 5% level of si~ifieance, only 6 Ss showed a predilection for one direction of gaze during one of the three kinds of questions. Two persons did this for two different questions, none for all three tasks. Four of them preferred the right side, four the left side.
Directional preponderance of saccadic activity As we had recorded the eye movements continuously, we calculated directional differences not only for the first saouide of ench interval, but also for the whole utccadic activity during the baseline phases and the questions. The different intetvale had different lengths of time. To be able to compare them, we averaged not the number, but the frequency of the saccades (see Table 2). As to the verbal questions, the shift of gaccadic activity to the left during the interval i3--it is significant. The mean values were also cakulated for the baseline phases, and for the total time of all questions; no significant differences were noted (see Table 3). Table 3. Directional preponderance during the baseline phase and the total time of the questions Frequency of sm__,~_~_,:l_cs Right Left Questions Baseline
8.3 6.4
8.2 6.7
W t
p
189 178
ns ns
Abbreviations see Table 2.
DISCUSSION In our experimental design we tried to avoid any cue that could lead to an asymmetric shift of eye movements. The subjects lay in complete darkness in a soundproof room. The questions were presented from directly behind, and the microphone that recorded the answers was placed centrally before the Ss. If there was any influence of cerebral laterality on the direction of the first eye movement following a question, it should have been detected under these conditiom. As shown previously, there was no significant influence found. This is in accordance with the EOG examination of HlscocK [15, 16] who also found no directional difference after his verbal questions (except some
subsets).
In contrast to our results, KtNsmOtnt~ [TJ, K o c ~ ez ai. lIT], GALIN and OnN~rlEIN [18], WEITEN and ETAUGH [19], Gtnt eta/. [20], SCXWARTZet al. E21] and Tucront and Sula E22] found more eye movements to the right following verbal questions. This difference can perhaps be explained by the methodological difficulties mentioned above, or by factors of the experimental situation which are dilTtcnlt to determine subsequently. This interpretation is emphaaized by the fact that only one half of the studies specifically concerned with lateral eye movements reported such a difference [51. Neither during the baseline phases nor during the entire time oftbe questions was there a difference between the frequency of eye movements to the right and to the left. If such a difference could have been shown, it would have been probable that there had been some "asymmetry factor" in our design which induced subjects to prefer one direction of gaze to another. Now it could be argued that we only scored movements to the right or to the left and that e.g. a preponderance of saccades to the le~ could well be saccades from the right back to the centre. Opposed to this arffunant are the results of B~cKER and KLEIN [23],who showed that eccentric fixation in the dark can hardly be maintained and that the normal position is the primary position.
NOTE
595
Our finding of a dire~ional preponderanee to the left during the interval i3-i4 of the verbal questions, can be described as a more frequently occurring deviation of the eyes to the left side in these intervals, followed by a return to the normal potation during i5 and the following il. As far as we are able to a.u:ertaln, neither neurologkal theories oan~,rning eye movement control, nor those about cerebral laterality offer an interpretation of this result. As we had "symmetrical" conditions, our expecimental design gives no hint, either. One explanation which the data suggests is that the cognitive structure, different for the three kinds of question, had an influence on the direction of the eye movements. Possible factors of this influence could he the difficulty of the task. the strategies of information processing and problem solving, and the control of the verbal output. How this influence could have been mediated is still unclear.
REFERENCES 1. TInTeLaAU~ H. Spontaneom rhythmic ocular movementL Their pmsible relationship to mental activity. Neurology 4, 350-354, 1954. 2. DAY, M. An eye movement phenomenon relating to attention, thousht, and anxiety. Percept. Mot. Skills 19, 443-446, 1964. 3. ELL~nCG, J. Blickverhalten und Sprechaktivitit. Phil. ~ Universitiit Marburg/Lahn 1975. 4. EL_tG~G, J. and CEARr~ A. Looking behavior: intended social signal or indicator of internal information processing. 1976 Meeting of the Animal Behavior Society--Human Ethology Meeting, Boulder, Colorado, 1976. 5. Eit~tCnMAN, H. and Wencal~oet, A. Lateral eye movements and hemispheric asymmetry: a critical review. Psychol. Bull. 8,5, 1080-1101, 1978.
6. BA~.^~P.Hypn~tizab~ity~aterality~feyem~vementsandfun~tionalbralnasymmetry.Percept.Mot.Skills2& 927-932, 1969. 7. Kl~mJotr~ra, M. Eye and head turning ~ t e s c~febral latetalisation. Scieace 176, 539-541, 1972. 8. Blzzt, E. Discharge of frontal eye field neurons during ~_e¢~lic and following eye movements in unanesthetized monkeys. E,xpl Brain res. 6, 69--80, 1968. 9. BlZZl, E. and S t r u n g , P. Single unit activity in frontal eye fields of unaaesthetized monkeys during eye and head movements. Expl Brain Res. 1O, 151-158, 1970. 10. M o x ~ , C., GOLDBm~.O,M. and WtntTZ, R. Visual receptive fields of frontal eye field neurons. Brain ICes. 61, 385-389, 1973. 11. la~twao~, K. H. and McGun,~ss, D. Arousal, activation, and effort in the control of attention. Psychol. Ray. 82, 116--149, 1975. 12. RAPttAN,T. and COHEN,B. Brainstem mechanisms for rapid and slow eye movements. Ann. Ray. Physiol. 48, 527-552, 1978. 13. FISCHER,H. and KOtlL~oF, M. Untersuchung der K6rperdominan~ Prax. Kinderpsychol. K~lerpsychiat. 5, 173-177, 1964. 14. CaAMON, D. VON and NL~BAUI~, H. Programmsystem zur automatischen Erkennung yon latefalen ~i~hen Augenbewegnngen und Lidbewegungen im Elektroocuiosramn~ EDVMed. Biol. 9, 96-100,1978. 15. HmCocK, M. Effects of examiner's location and subject's anxiety on gaze laterality. Neuropsycholooia 15, 409-416, 1977a. 16. ~ , M. Eye movement asymmetry and hemispheric function. An examination of individual differenees. J. Psychol. 97, 49-52, 1977b. 17. KOO~, K., GAtJN, D., ORr4STmN,R. and M ~ , E. Lateral eye movement and cognitive mode. Psychonomic $ci. 27, 223-224, 1972. 18. GAL~, D. and Ol~m, elN, R. Individual differen~s in cognitive style---I. Reik~ive eye movements. NeuropsychoJooia, 12, 367-376, 1974. 19. Wus.ea~,W. and ETAUGH,C. Lateral eye movements as a function ofcognitive mode, questionsequenee, and sex of subjects. Percept. Mot. Skills 38, 4~9 A~A,1974a. 20. Gtnt, R. E., GuR, R. C. and HArms, L. Cerebral activation as measured by subjects' lateral eye movements, is influenced by experimenter location. Neuropsycholooia 13, 35--44, 1975. 21. SCHWARTZ,G., D^vn3soN, R. andM~el~, F. Right hemisphere lateralisation for emotion in the human brain: intera¢'tions with cognition. Science 190, 286-288, 1975. 22. T u ~ , G. and Sure, M. Conjugate lateral eye movement (clam) direction and its relationship to performance on verbal and visuoepatial tasks. Neuropsychologia 16, 251-254, 1978. 23. B e ~ , W. and Kurus, H. Accuracy of saccadic eye movements and maintenance of eccentric eye position in the dark. Vision Res. 13, 1021-1034, 1973.
596
NOTE R6sum6 : Par enregistrement des mouvements oculalres lat6raux dos suJets ayant los youx ouvorts darts l'obscurit~, on ne pouvalt pas d6toctor d'Influonce du type d'~prouve sur le premier mouvement oculalro aprls la question. Une analyse de l'onsemble des .~uvements oculalros mon~ralt une pr6pond6ranco dlrectionnelle vers la gauche lots do cortalnos parties des ~prouves verbales.
Die
lateralen
offcnen Ein
Augen
Einflu~
Augenbewcgungen
yon
in c i n c m
l~um
der
Aufgabe
dunklen auf
die
Versuchspcrsoncn, bcfandcn,
Richtung
dcr
wurden erstcn
die
sich
mit
rcgistricrt. au£
dic
Fragc
f o l g e n d e n Augcnbewegungen I i e ~ s i c h n i c h t f c s t s t c l l e n . Einc Analyse aIIer Augenbcwc~ngen zcigt cin Richtungsfibcrwiegcn nach links w~hrend e i n z e l n e r A b s c h n l t t e der v e r b a l e n Aufgaben.
0028-3932/80/1001--0591 $02.00/0
NOTE IS THERE AN INTERACTION BETWEEN COGNITIVE ACTIVITY A N D LATERAL EYE MOVEMENTS? WOLFGANG S~UNG and DETLEV VON C~,AMON
Abteilung ffir experimentefle Nenrologie, Max-Planck-Institut fur Psychiatric, D-8000 Mfinchen 40, Kraepelinstra~ I0 (Received 11 February 1980) Almraet--recording lateral eye movements of Ss with eyes opened in a dark room, no influence of the task on the first eye movement following the question could be detected. An analysis of all eye movements showed a directional preponderance to the left at certain parts of the verbal tasks.
SINCE the first works of'rgd'rEt.gAUMEli and DAY [2], the relationship of lateral eye movements following a question to information processing ['l, 3, 4], several individual differences and, more importantly, to cerebral lateralisation have been the subject of a great number of publications (for references see the review of Em~ICt[MA~ and W~OU, [5]. However, the two main problems arising from these articles have been the hypothesized relationship between hemispheric asymmetry and the direction of eye movements, and the diffgulties involved with the qmmtions and methods used for examination. A theory concerning the intera~ion between cerebral activation and a deviation of Ilaze directed contralaterally to the "active" hemisphere was first proposed by BAKAN [6]. He thought that as eye movements were controlled contralaterally by activity in the "frontal eye field" (Brodman area 8), the left- or right-movement could be "symptomatic of easier triggering of activities in the hemisphere contralateral to the direction of eye movement". KINSDOURNE[7] modified this model He proposed that as "the cerebrum is a highly linked system", verbal activation could overflow into the left-sided orientation center, "driving attentional balance off center and to the right". Recent papers have seldom tried to reconsider these theories in the light of new neuroanatomical mad neurophysiological findings. These findings showed that area 8 does not specifically control the direction of eye movements [8, 9, I0]. The model of Kinsbournc of an "overflow" of activation to an "orienting center" likewise seems much too simplified [ 11"]. "How the central nervous system generates saccades is still speculative" (RAPHAN and CottoN, 1"12]). As Etmt.iCnMAN and Wu~mJmou [5] recently offered a very detailed analysis of the theoretical research concerning "lateral eye movements" and of the methodological problems involved, we confine ourselves to a short comprehensive summary of their work. The main difficulties are: (a) the situation: to what extent does the field of vision, the localisation of the experimenter, and the acoustical background influence the direction of eye movements? (b) the recording and g o r i n g of the eye movements: which movements are to be recorded, and which method of recording should be used? Should stares and vertical eye movements be included? (c) the kind of the questions asked; do they mainly activate only one hemisphere? In accordance with EHm.ICM~N and W m m m ~ c ~ [5], we started from the consideration that there is no reason to presume that the influence of a question would result only in a deviation of the first eye movement. If all environmental factors that could lead to a directional shift are (as far as possible) excluded, then any influence should be detectable.
METHODS Subjects Thirty persons (18 women, 12 men) between 16 and 30 years ofage served as subjects. Their handednes$ was tested by eight different tasks [13]; 27 persons were right-handed, 2 left-handed and 1 person left-handed as a child was now right-handed. The subjects were told that the experiment was to measure their ability to concentrate in darkness, and that an EEG would be recorded. 591
592
NOTE
Materials Three kinds of questions were used: 30 verbal questions [the Ss had to build a sentence of two words (randomlypaired German words, containing one or two syllables)]; 30 arithmetical questions (multiplication of a one-digit number by a two-digit number between 10 and 20); and 30 musical questions (Ss had to hum four tones in imitation of a flute).
Situation During the experiment, Ss lay on a bed in a room 3.5 m x 2.5 m x 2.2 m. The room was completely dark (confirmed by all Ss). Their head was fixed in a normal position, so as to avoid a superpmition of eye and head movements. The Ss were instructed to keep their eyes open during the whole semion (this was supervised by the experimenter). The soundproof room was screened from possible electrical disturbances, the only sound continuously heard was the buzzing of an air-conditioner keeping temperature and atmospheric moisture constant. The questions were presented from a tape-recorder through a loudspeaker located directly behind the S's head. The responses of the Ss were transmitted to the experimenter outside the room by means of a microphone.
Desujn of the experiment Each question was divided into five parts: an interval it (before the question), interval i2 (question), interval i3 (the S "solves" the problem), interval i4 (answer) and interval i5 (fixed interval after the answer). Figure I shows this. The beginning of each interval was recorded by the experimenter who gave different trigger signals to the computer being used (PDP 11/40). The experiment began with five minutes of a first baseline (Ss were instructed to lie silently), then came the first block of 45 questions, randomly divided into 15 verbal, 15 arithmetical and 15 musical questions. Then came another baseline, then the second block with again 45 questions, and then the third baseline. Each baseline took 5 minutes; each block about 15 minutes. The beginning and the end of each block and each baseline were also recorded.
Subject is awaiting the quest ion
,
~
listening to the question
,,
~'N
answering
thinking
,,
A
"
~
'
i,,
sa
I
i ,, i
fixed inter-about 3 vai a f t e r sec untJ[ the end of the next the ,~nsww question
Fro. 1. Temporal soquence of a question.
Apparozus and recording The eye movements of the Ss were recorded continuously by an electrooculogramm (EOG). Four channels (each eye was monitored horizontally and vertically) were A-C recorded (time constant 5 seconds) on a Beckman Dynograph, using s/lvet,-e/Iver chloride electrodes (skin resistance below 5 k~). The recorded signals were given to the computer, which was programmed to identify sazcadic eye movements [14]. Only saccades with an amplitude of more than 5° and with a maximum angular velocity of more than 180°/sec were scored, thus excluding "noise" and slow dril~ movements from the analysis. With the help of the trigger signals indicating the relevant points of time, the eye movements of the Ss could be calculated for each interval.
Scormo of the eye movements We limited our analysis to the horizontal s~_cc~_des,or the horizontal components of vertical and oblique saccades. The way of recording used in this experiment did not register a constant zero-line, i.e. the ~ . d i r e c t i o n "straight on" could not be defined unequivocally; in addition, saccades from different starting-points are only comparable to a limited degree. Therefore, we only scored eye-movements going to the right or to the left in relation to their previous position.
24.7 12.6 25.9 16.6 21.9 30.3 30.9
il i2 i3 i4 i5 i2-4 i3-4
22.2 13.0 33.4 20.7 14.9 41.4 38.7
% Left 53.1 74.4 40.7 62.8 63.1 28.2 30.4
184 177 168 157 129 141 157
Verbal questions % None t W
ns ns ns us 5% ns ns
P 26.8 11.2 21.2 6.7 17.6 28.4 23.4
% Right 24.7 14.3 20.3 8.0 15.2 28.4 24.7
48.6 74.4 58.4 85.3 67.2 43.1 51.9
212 209 231 208 184 225 214
Arithmetical questions % % Left None t W
ns ns ns ns ns ns ns
P
8.1 5.4 9.1 8.7 9.5 8.3 9.2
8.3 5.3 10.8 10.3 7.2 9.4 10.7
210 193 160 151 134 122 117
Verbal questions Frequency of saecades Right Left t W
ns ns ns ns 5% 5% 2%
p 9.6 5.2 7.2 8.1 8.9 6.3 7.1
8.9 6.0 7.8 8.1 7.3 7.0 7.7
177 193 193 160 165 171 193
Arithmetical questions Frequency of saccades W Right Left t
Freque~y of saccades: values calculated per minute; Right, Left: saccades to the right or the left. W: Wilcoxon Test (see Table 1). il-i5: the intervals of each question (see Fig. 1).
il i2 i3 i4 i5 i2--4 i3-4
Intervals
ns ns ns ns ns ns ns
p
Table 2. Directional preponderance of saccades of each interval
% Right, ~o Left: percentage of lateral eye movements to the right and to the left. % None: percentage of intervals where no saccade was made. W: result of the Wilcoxon Test, t: t-values, p: level of significance (as: not significant, 5%: significance of 5 %l il-5: the intervals of each question (see Fig. 1).
% Right
Intervals
Table 1. Direction of the first lateral eye movement of each interval
29.4
21.8 14.2 22.3 19.1 20.7 35.7
% 51.1 72.6 65.2 59.0 57.8 37.1 43.0
None
8.8 4.7 9.1 10.1 10.4 7.5 9.8
7.6 4.9 13.4 9.5 9.2 8.3 10.8
143 214 149 205 191 188 189
Musical questions Frequency of saccades Right Left t
27.1 13.2 12.4 21.9 21.6 27.2 27.5
Left
Right
Musical questions
%
%
W
209
161 198 138 205 218 178
t
w
ns ns ns ns us ns ns
p
ns
ns ns ns ns ns us
UJ
Z
594
NOTE
RESULTS Direction of the.~rst saccade of each interval For each interval of the question, we tested whether a ~__~__dehad been made, and in which direction the first saccade occurred. In order to have data comparable to those presented in the studies concerning lateral eye movements, we alao tested the combined intervals D-it and i2-i4. The combined interval i3-it represents the first eye movement following the end of the question, and the combined interval i2-it, the first eye movement following the beginning of the question (a value also scored in some papers). Table 1 gives the percentage values of'first __~,~_ _~es" in each interval directed to the right or to the left, and the proportion ofintervala without eye movements. In order to obtain the diffegencm of these values, the Wilcoxon Test was calculated over the mean values of each person (i.e. each value represented the mean of the 30 questions of each kind the Ss were asked). During the relevant intervals i2, i3, it, no significant differences appeared. Additionally, we calculated the differences for the individual data for the combined interval i3-it by means of the Binominai Test. On a 5% level of si~ifieance, only 6 Ss showed a predilection for one direction of gaze during one of the three kinds of questions. Two persons did this for two different questions, none for all three tasks. Four of them preferred the right side, four the left side.
Directional preponderance of saccadic activity As we had recorded the eye movements continuously, we calculated directional differences not only for the first saouide of ench interval, but also for the whole utccadic activity during the baseline phases and the questions. The different intetvale had different lengths of time. To be able to compare them, we averaged not the number, but the frequency of the saccades (see Table 2). As to the verbal questions, the shift of gaccadic activity to the left during the interval i3--it is significant. The mean values were also cakulated for the baseline phases, and for the total time of all questions; no significant differences were noted (see Table 3). Table 3. Directional preponderance during the baseline phase and the total time of the questions Frequency of sm__,~_~_,:l_cs Right Left Questions Baseline
8.3 6.4
8.2 6.7
W t
p
189 178
ns ns
Abbreviations see Table 2.
DISCUSSION In our experimental design we tried to avoid any cue that could lead to an asymmetric shift of eye movements. The subjects lay in complete darkness in a soundproof room. The questions were presented from directly behind, and the microphone that recorded the answers was placed centrally before the Ss. If there was any influence of cerebral laterality on the direction of the first eye movement following a question, it should have been detected under these conditiom. As shown previously, there was no significant influence found. This is in accordance with the EOG examination of HlscocK [15, 16] who also found no directional difference after his verbal questions (except some
subsets).
In contrast to our results, KtNsmOtnt~ [TJ, K o c ~ ez ai. lIT], GALIN and OnN~rlEIN [18], WEITEN and ETAUGH [19], Gtnt eta/. [20], SCXWARTZet al. E21] and Tucront and Sula E22] found more eye movements to the right following verbal questions. This difference can perhaps be explained by the methodological difficulties mentioned above, or by factors of the experimental situation which are dilTtcnlt to determine subsequently. This interpretation is emphaaized by the fact that only one half of the studies specifically concerned with lateral eye movements reported such a difference [51. Neither during the baseline phases nor during the entire time oftbe questions was there a difference between the frequency of eye movements to the right and to the left. If such a difference could have been shown, it would have been probable that there had been some "asymmetry factor" in our design which induced subjects to prefer one direction of gaze to another. Now it could be argued that we only scored movements to the right or to the left and that e.g. a preponderance of saccades to the le~ could well be saccades from the right back to the centre. Opposed to this arffunant are the results of B~cKER and KLEIN [23],who showed that eccentric fixation in the dark can hardly be maintained and that the normal position is the primary position.
NOTE
595
Our finding of a dire~ional preponderanee to the left during the interval i3-i4 of the verbal questions, can be described as a more frequently occurring deviation of the eyes to the left side in these intervals, followed by a return to the normal potation during i5 and the following il. As far as we are able to a.u:ertaln, neither neurologkal theories oan~,rning eye movement control, nor those about cerebral laterality offer an interpretation of this result. As we had "symmetrical" conditions, our expecimental design gives no hint, either. One explanation which the data suggests is that the cognitive structure, different for the three kinds of question, had an influence on the direction of the eye movements. Possible factors of this influence could he the difficulty of the task. the strategies of information processing and problem solving, and the control of the verbal output. How this influence could have been mediated is still unclear.
REFERENCES 1. TInTeLaAU~ H. Spontaneom rhythmic ocular movementL Their pmsible relationship to mental activity. Neurology 4, 350-354, 1954. 2. DAY, M. An eye movement phenomenon relating to attention, thousht, and anxiety. Percept. Mot. Skills 19, 443-446, 1964. 3. ELL~nCG, J. Blickverhalten und Sprechaktivitit. Phil. ~ Universitiit Marburg/Lahn 1975. 4. EL_tG~G, J. and CEARr~ A. Looking behavior: intended social signal or indicator of internal information processing. 1976 Meeting of the Animal Behavior Society--Human Ethology Meeting, Boulder, Colorado, 1976. 5. Eit~tCnMAN, H. and Wencal~oet, A. Lateral eye movements and hemispheric asymmetry: a critical review. Psychol. Bull. 8,5, 1080-1101, 1978.
6. BA~.^~P.Hypn~tizab~ity~aterality~feyem~vementsandfun~tionalbralnasymmetry.Percept.Mot.Skills2& 927-932, 1969. 7. Kl~mJotr~ra, M. Eye and head turning ~ t e s c~febral latetalisation. Scieace 176, 539-541, 1972. 8. Blzzt, E. Discharge of frontal eye field neurons during ~_e¢~lic and following eye movements in unanesthetized monkeys. E,xpl Brain res. 6, 69--80, 1968. 9. BlZZl, E. and S t r u n g , P. Single unit activity in frontal eye fields of unaaesthetized monkeys during eye and head movements. Expl Brain Res. 1O, 151-158, 1970. 10. M o x ~ , C., GOLDBm~.O,M. and WtntTZ, R. Visual receptive fields of frontal eye field neurons. Brain ICes. 61, 385-389, 1973. 11. la~twao~, K. H. and McGun,~ss, D. Arousal, activation, and effort in the control of attention. Psychol. Ray. 82, 116--149, 1975. 12. RAPttAN,T. and COHEN,B. Brainstem mechanisms for rapid and slow eye movements. Ann. Ray. Physiol. 48, 527-552, 1978. 13. FISCHER,H. and KOtlL~oF, M. Untersuchung der K6rperdominan~ Prax. Kinderpsychol. K~lerpsychiat. 5, 173-177, 1964. 14. CaAMON, D. VON and NL~BAUI~, H. Programmsystem zur automatischen Erkennung yon latefalen ~i~hen Augenbewegnngen und Lidbewegungen im Elektroocuiosramn~ EDVMed. Biol. 9, 96-100,1978. 15. HmCocK, M. Effects of examiner's location and subject's anxiety on gaze laterality. Neuropsycholooia 15, 409-416, 1977a. 16. ~ , M. Eye movement asymmetry and hemispheric function. An examination of individual differenees. J. Psychol. 97, 49-52, 1977b. 17. KOO~, K., GAtJN, D., ORr4STmN,R. and M ~ , E. Lateral eye movement and cognitive mode. Psychonomic $ci. 27, 223-224, 1972. 18. GAL~, D. and Ol~m, elN, R. Individual differen~s in cognitive style---I. Reik~ive eye movements. NeuropsychoJooia, 12, 367-376, 1974. 19. Wus.ea~,W. and ETAUGH,C. Lateral eye movements as a function ofcognitive mode, questionsequenee, and sex of subjects. Percept. Mot. Skills 38, 4~9 A~A,1974a. 20. Gtnt, R. E., GuR, R. C. and HArms, L. Cerebral activation as measured by subjects' lateral eye movements, is influenced by experimenter location. Neuropsycholooia 13, 35--44, 1975. 21. SCHWARTZ,G., D^vn3soN, R. andM~el~, F. Right hemisphere lateralisation for emotion in the human brain: intera¢'tions with cognition. Science 190, 286-288, 1975. 22. T u ~ , G. and Sure, M. Conjugate lateral eye movement (clam) direction and its relationship to performance on verbal and visuoepatial tasks. Neuropsychologia 16, 251-254, 1978. 23. B e ~ , W. and Kurus, H. Accuracy of saccadic eye movements and maintenance of eccentric eye position in the dark. Vision Res. 13, 1021-1034, 1973.
596
NOTE R6sum6 : Par enregistrement des mouvements oculalres lat6raux dos suJets ayant los youx ouvorts darts l'obscurit~, on ne pouvalt pas d6toctor d'Influonce du type d'~prouve sur le premier mouvement oculalro aprls la question. Une analyse de l'onsemble des .~uvements oculalros mon~ralt une pr6pond6ranco dlrectionnelle vers la gauche lots do cortalnos parties des ~prouves verbales.
Die
lateralen
offcnen Ein
Augen
Einflu~
Augenbewcgungen
yon
in c i n c m
l~um
der
Aufgabe
dunklen auf
die
Versuchspcrsoncn, bcfandcn,
Richtung
dcr
wurden erstcn
die
sich
mit
rcgistricrt. au£
dic
Fragc
f o l g e n d e n Augcnbewegungen I i e ~ s i c h n i c h t f c s t s t c l l e n . Einc Analyse aIIer Augenbcwc~ngen zcigt cin Richtungsfibcrwiegcn nach links w~hrend e i n z e l n e r A b s c h n l t t e der v e r b a l e n Aufgaben.