Nampsychologia, Vol. 16, pp. 653 to 657. 0 Pergamon Press Ltd. 1978. Printed in England.
NOTE EFFECTS
OF VOLUNTARY EYE MOVEMENTS ON HEMISPHERIC ACTIVITY AND CHOICE OF COGNITIVE MODE YIGAL GROSS,RACHELFRANKO and ISAACLEWIN
Department
of Psychology, Bar-Ilan University, Ramat-Gan,
Israel
(Received 24 April 1978)
Ah&act-The present study tests the hypothesis that voluntary lateral eye movements produce heightened arousal in the contralateral hemisphere. A task which can be performed using either the semantic or the non-semantic cognitive mode was presented to subjects who were directing their gaze either to their right or their left. Forty right-handed subjects preferred the non-semantic mode more often while gazing to the left than while gazing to the right. No such effect was detectable with left-handed subjects. It is concluded that hemispheric activity can be affected by voluntary lateral gaze. EACH of the two cerebral hemispheres
is known to specialize in different types of cognitive processing. The “dominant” hemisphere is specialized for semantic, propositional, analytic processing while the other, the “minor” hemisphere, is specialized for non-semantic, appositional, holistic, contigurational processing (e.g. [l, 21). This functional difference has been established by various methods, including the testing of patients with accurately localized brain injuries [3, 41, the testing of processing of input directed to one hemisphere primarily by the dichotic listening technique [5, 6], and by a thorough investigation of a few split brain patients [7-g]. A recent significant contribution to the study of hemispheric specialization is the demonstration that there is a systematic relationship between which of the two hemispheres is the more active and the direction of the lateral movements of the eyes while reflecting [lo]. The Crst investigators to establish this relationship thought it might provide a new means of clarifying some individual differences. An individual could thus be classified as either a “right mover” or a “left mover” depending on the predominant direction to which his eyes move when he reflects. Some individual differences such as reading speed [lo] and hypnotizability [l l] have been related to the subject’s being a right or a left mover. Other investigators directed their attention to the relationship between the lateral eye movements and the temporary predominance of one hemisphere which depends on the kind of cognitive processing being done at a given moment [12,13]. This relationship occurs only with right-handers, but not with left-handers whose lateralization of functions is known to be variable and not well understood [14]. It is important to note that the lateral direction of the eye movements depends less on the nature of the input than on the type of cognitive processes which are required [13]. Further support for the relationship between the lateral eye movements and hemispheric activity is provided by the following two facts: (1) A spatial task is performed better when a right-handed subject’s eyes involuntarily move to the left than when they move to the right, presumably due to correspondence between task requirements and relative amount of arousal in the two hemispheres [15]; and (2) While engaged in verbal processing, a right-handed subject is more attentive to the right side of his visual field and to the right side of figures presented to him than under standard conditions [13]. On the basis of the last findings and other data, KINSBOURNE[13] presents an attentional model to explain the relationship between temporary hemispheric preference and lateral eye movements. According to this model, each hemisphere programs the synergic eye and head movements towards the contralateral direction. The highly linked organization of each hemisphere permits signiticant crosstalk between lateralized higher mental functions and the orienting control mechanism on the same side. AS a result, visual attention becomes biased toward contralateral space, not for the purpose of information retrieval, but secondary to the asymmetrical cortical activity. The model suggests an induction or generaliition of arousal within a hemisphere. Arousal produced by a cognitive task in a given area overflows, so to speak, to other areas within the same hemisphere. Given the above information, does the reverse causal relationship also exist? Can lateral attention be 653
654
NOTE
induced by voluntary lateral eye movements which in turn will induce relative heightened arousal of the contralateral cerebral hemisphere? The above hypothesis has been partially supported in a recent experiment [16] in which subjects were taking cognitive tests while wearing safety goggles taped so as to force them to look to the required side. The main result of the above experiment is that left-looking subjects tend to do better on creativity and spatial tasks as compared with right-looking ones. The purpose of the present report is to investigate further the relationship between voluntary eye movements and cognitive functioning by using another task and by comparing the results of left-handed subjects to those of right-handed subjects. The involvement of hemispheric arousal in the effects of voluntary lateral eye movements on cognitive functions will be clearly demonstrated by comparing the performance of righthanders to that of left-handers in the experiment described below.
METHOD Materials Two lists (A and B) of 15 sets of three Hebrew words each were prepared according to the following guidelines: Each of ten of the 15 sets in both lists contained two synonyms and a third word which was a rhyme to one of them. An English example of such a set would be: WATCH, CLOCK, BLOCK. The middle word was always the synonym to one of the other two and the rhyme to the remaining word. In half of the sets the synonym was presented first and the rhyme third; in the other half the order was reversed. The order in each set was decided at random. Four of the remaining five sets (placed in positions 1,2,4, and 10) on both lists included 2 rhyming words each. One set (placed in position 3) included two synonyms. The third word in each of these five “unidimensional” sets was neither synonymous nor similar in sound to the other two words. Subjects The subjects were 40 right-handed and 20 left-handed university and yeshiva male students. subjects were fluent Hebrew speakers and volunteered to participate in the experiment.
All the
Procedure Each subject was tested individually in a room which was as symmetrical as possible. The experimenter instructed the subject to direct his gaze to the desired side (left or right) and fitted him with earphones through which one of the two lists was to be presented binaurally with equal intensity to each ear. The subject was then instructed to listen to the sets of words and to choose and say aloud the odd word of each set. At the end of the first list, the subject was instructed to direct his gaze to the other side and the same procedure was then followed with the second list. List A was presented first to half of the subjects and list B was presented first to the other half. The experimenter sat behind the subject during the testing since the presence of the experimenter in front of the subject has been shown to interfere with a related task [14]. Actual monitoring of the subject’s eye movements was technically difficult and was not done. Half of the subjects directed their gaze to the right while responding to the first list presented to them, the other half to the left. The experimenter recorded the subject’s choice after each of the 10 two-dimensional sets. While performing the task, the subject was therefore free to choose whether to concentrate on the objects to which the words refer, a semantic function for which there is a left hemisphere superiority, or to choose to emphasize the contigurational, auditory appearance of the words. The latter non-semantic processing mode is most likely subserved by the right hemisphere. The five unidimensional sets were introduced in order to direct the subject’s attention to both possibilities and were not included in the data.
RESULTS The frequency distributions of number of non-semantic responses for each group in each condition are presented in Fig. 1, and the related mean number of non-semantic responses are presented in Table 1. The Table 1. Mean number of non-semantic responses in the two handedness groups under each of the two experimental conditions and relevant P values Direction of gaze Left Right P
Handedness Left-handed Right-handed 2.5 0.7 0.8 0.7 N.S. < 0.01
P < 0.01 N.S.
NOTE RIGHT
0
2
655 HANDERS
8
4
NO OF6 NO; - Sk’MiNT,;:
LEFT
IO
REkPOiSES
HANDERS
15
LEFT
NO
FIQ. 1. Frequency
GAZE
OF
NON - SEMANTIC
RIGHT
GAZE
i
RESPONSES
distributions of non-semantic responses in the two handedness under each of the two experimental conditions.
groups
data were analyzed using the Mann-Whitney U test and the Wilcoxon Matched Pairs Signed Ranks test [17]. The relevant P values are also presented in Table 1. Inspection of the data reveals that the results produced by the right-handed groupin the “left gaze” condition differ signiticantly from the other three results, namely, those produced by the same group in the “right gaze” condition and those produced by the left-handed group in both conditions. These three results are practically identical both in terms of their means and their frequency distributions.
DISCUSSION The results demonstrate conclusively that the cognitive processing of right-handed subjects is significantly affected by the direction to which they look. Left-handed people, however, are not affected by the treatment. Since the treatment a&ted the right-handed subjects but not the left-handed subjects, it seems plausible that when a right-handed subject directs his eyes to one side, the contralateral cerebral hemisphere is aroused and the cognitive processes which are localized within that hemisphere gain predominance. Rinsbourne’s attentional model is thus supported. The model should, however, be tested further by experimentally manipulating some features of the lateral gaze. For example, Kinsboume’s attentional model should lead to a prediction that the experimental effects of lateral gaze will be strengthened if the subject is required to direct visual attention (not merely gaze) to one side. Likewise, the effects should be augmented by arousing the desired hemisphere through the direction of attention of other sensory modalities, in addition to the visual modality, to one side of the perceptual space Our results seem to contrast sharply with Levy and Traverthen’s conclusion that there is a left hemisphere dominance for rhyming [18]. However, inspection of the task used by Levy and Traverthen reveals that it confounded two different aspects: (a) naming pictures of objects; and (b) identifying those pictures whose names rhyme. It is clear that the execution of the second part of the task is dependent on the naming which is known to be a left hemisphere function. Levy and Traverthen’s work does not lead, therefore, to the conclusion that rhyming as such is a left hemisphere function. The possibility of affecting the balance between the two hemispheres is of a potential, practical importance as well, provided the effects are strong enough, particularly since the required procedure is so extremely simple. It is possible that such a method could be used in order to help subjects concentrate for a longer time on a given task. Thus, it is possible that making the subject look in the desired direction while he is performing the task, and in the other direction when he relaxes, will increase his efficiency. A similar possibility is to help subjects who have problems in concentrating their attention (e.g. retarded children) to do so efficiently by arousing differentially one of their hemispheres. Another line of investigation is to use the present method to enhance desired cognitive functions such as differentially enhancing verbal or non-verbal memory. Some of these points are presently under investigation in our laboratories.
656
NOTE
Acknowledgements-The authors would like to express their gratitude helped them solve some statistical problems, to Mrs. B. SINGERwho and to Drs. E. K. WARRINGTONand H. GLAUBMAN who commented The study presented here was funded through the Research Committee
to Drs. S. Fox and M. SNEIDERwho took part in editing the manuscript, on an earlier version of this paper. of Bar-Ban University.
REFERENCES 1.
BOGEN, G. E. The other side of the brain-II.
An appositional mind. Bull. Los Ang. neural. Sot. 34, 135-162,1969. 2. KIMURA, D. The asymmetry of the human brain. Scient. Am. 228,70-79,1973. 3. DE RENZI, E., FAGLIONI,P. and SCOTTI,G. Tactile spatial impairment and unilateral cerebral damage. J. Nerv. Ment. Dis. 146.468. 1968. 4. DE RENZI, E. and SP&&R~ H. Facial recognition in brain-damaged patients. Neurology 6, 145-152, 19661~. 5. KIMURA,D. Functional asymmetry of the brain in dichotic listening. Cortex 3,163-l 78,1967. 6. HINES, D. and SATZ, P. Superiority of right visual half-fields in right-handers for recall of digits presented at varying rates. Neuropsychologia 9, 21-25, 1971. 7. MILNER, B. and TAYLOR,L. Right-hemisphere superiority in tactile pattern recognition after cerebral commissurotomy: evidence for nonverbal memory. Neuropsychologia 10, 1, 1972. 8. NEBES,R. D. Hemispheric specialization in commissurotomized man. Psychol. Bull. 81, l-14, 1974. 9. SPERRY,R. W. Lateral specialization in the surgically separated hemispheres. In: The Neurosciences: Third Study Program, F. 0. SCHMITTand F. G. WARDEN (Editors). M.I.T. Press, Cambridge, 1973. 10. BAKAN, P. and SHOTLAND,R. L. Lateral eye-movement, reading speed, and visual attention. Psychon. Sci. U(2), 93-94, 1969. 11. BAKAN,P. Hypnotizability, laterality of eye-movements and functional brain asymmetry. Percept. Mot. Skills 28,927-932, 1969. M. Eye and head turning indicates cerebral lateral&ion. Science, N. Y.176,539-541,1972. 12. KINSBOLJRNE, 13. KINSBOURNE,M. The control of attention by interaction between the cerebral hemispheres. Attention and Performance--IV. S. KORNBLUM(Editor), pp. 239-256. Academic Press, London, 1973. 14. H~~CAEN, H. and SAUGET,J. Cerebral dominance in left-handed subjects. Correx 7,19-48,1971. 15. GUR, R. E., GUR, R. C. and HARRIS, L. J. Cerebral activation as measured by subjects’ lateral eye movements is influenced by experimenter location. Neuropsychologia 13(l), 35-44197.5. 16. HINES, D. and MARTIMIALE,C. Induced lateral eye movements and creative and intellectual performance. Percept. Mot. Skills 39, 153-154, 1974. 17. SIEGEL,S. Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York, 1956. 18. LEW, J, and TREVARTHEN,C. Perceptual, semantic and phonetic aspects of elementary language processes in split brain patients. Brain 100, 104-l 18, 1977.
Cette etude teste l'hypothke oculaires
lat6raux volontaires
selon laquelle les mouvements
accroissent
l'dveil de 1'hfmisphSre
con-
trolat6ral. Des sujets devaient rdallser une tdche qui pouvait Btre accomplie selon un mode cognitif soit semantique soit non s&nantique et la direction
laterale de leur regard etait observge.
pr6feraient
plus souvent le mode non semantique
40 sujets droitiers
lorsqu'ils regardaient
vers la gauche que lorsqu'ils regardaient vers la droite. Aucun effet de ce genre n'a et6 trouve chez les gauchers. On en conclut que l'activite h6mispherique
peut etre affectee par le regard volontaire
lateral.
NOTE
Deutschsorachige Zusammenfassunp: Die vorliegende Studie untersucht die Hypothese, daS will!riirliche seitliche Augenbewe,ugen eine verstarkte (elektrische) Erregung in der kontralateralen Hemisphsre hervorrufen. Eine Aufgabe, die mittels eines semantischen oder eines nichtsemantischen kognitiven Modus durchgefiihrtwerden kann, wurde Versuchspcrsonen dargeboten, die ihren Blick entweder nach rechts oder links hinwandten. 40 Rechtshgnder bevorzugten den nicht-semantischen Modus haufiger, wahrend sie nach links blickten als beim Blick nach rechts. Kein derartiger Effekt war bei linkshdndigen Probanden feststellbar. Es wird daraus geschlossen, daR die Hemisph5renaktivit~t durch willkiirliche seitliche Blickbewegungen beeinfluSt werden kann.