Conjugate lateral eye movements in Pan troglodytes

NOTE COKJUGATE

LATERAL

EYE

MOVEMENTS

CHARIT\ R. O'NEIL.H T. Rob STRATTOI\.ROBEIU Department nf Psycholngy. University of Oklahoma.

(Received

IN

PAN

TROGLODYTLA

H. INGERSOLL and Norman.

Oklahoma

RCGER

S.FOL~TS

73069.

U.S.A.

1 Jic/_~,,1978)

:Ihstract--The direction of conjugate lateral eye movements was assessed in four Juvemle and four adolescent chimpanzees (Pan troglodwes). A significant bias in favor of left eye movements was found in the two older adolescents. Neither the two younger adolescents nor the four juveniles revealed a significant asymmetry in the direction of conjugate lateral eye movements. The data suggest that mature members of this species so closely related to man may dcmonstrate a bias in hemispheric activation similar to that demonstrated by Homo .sopiens. laterality and hemispheric specialization in Homo sapiens have generated speculation regarding the uniqueness of the asymmetrical cerebral activity found in the human species. In human children, cerebral laterality has generaliy been assumed to be related to maturational factors, since stable hand preference (which is taken as evidence of cerebral dominance) does not seem to develop until the age of 4 yr or later [l-3]. The overwhelming preponderance of right-handedness in humans has prompted rather extensive research into the relationship hetween handedness and various aspects of cerebral activity [4]. The split-brain studies [5,6] were among the first to indicate specialization of the cerebral hemispheres for different cognitive functions. One consequence of these studies has been the widely held belief that language activities are relegated to the left hemisphere in most humans, regardless of handedness. Subsequent to the success of several projects involving the acquisition of language-like behavior by chimpanzees [7-lO],the possibility has been raised that functional cerebral asymmetry may also occur in certain closely related non-human species. ST~JDIES of cerebral

YENI-KOMSHIAX and BENSON [II] investigated anatomical asymmetries in various primate brains and found that the left Sylvian fissure was longer than the right in humans and that this fissure showed a similar,

but less pronounced, asymmetry in the chimpanzee brain, but no such asymmetry in the rhesus brain. Asymmetrical cerebral functioning has been demonstrated in monkeys by DEW~~N (121, who discovered that lesions in the left auditory association cortex produced a deficit in delayed match-from-sample performance, while comparable right sided lesions did not. To date, the only evidence for functional cerebral asymmetry in chimpanzees derives from studies of hand preference in this species. FiNCH [I 31 found handedness in 15 out of 30 chimpanzees (most of whom were adult), with equal incidence of right and left hand preferences. CHORAZYXA [14] reports shifts in hand preference in a young chimpanzee from the age of 3 days to 17 months. the first indications of hand preference appearing at 15 weeks of age. One index of ongoing hemispherical activity which is readily accessible in human subjects is the direction of conjugate lateral eye movements. PENFIELD and ROBERTS [15] determined that electrical stimulation of one hemisphere results in movement of both eyes in the direction opposite from the side stimulated. Since then, other researchers 116, 171 have reported that face-to-face questioning of a subject results in a break in gaze, foliowed by spontaneous lateral eye movements which are remarkably consistent in direction for a given subject. BAEAN [18] estimates that for the average person, 757; of conjugate lateral eye movements (CLEMs) are in the same direction, “right movers” and “left movers” being equally distributed in the population. GUR [19] assesses CLEMs as indicative of “hemisphere activation bias”. No relationship has been found between hand preference and the direction of CLEMs. The present study examined the direction of CLEMs in juvenile and adolescent chimpanzees. The hypothesis was that mature specimens of man’s fellow primate. Papr truglodyfrs, would reveal a bias in hemispheric activation similar to that displayed by Horn rnpiem$. METHOD The subjects were four juvenile (mean age 5 vr, 2 months) for four adolescent (mean age 11 yr, 1 month) chimpanzees (PO/~ fro,el&fes) at the Institutefor Primate Studie< associated with the University of Okla-

760

Non

homa.The juvenile group included two males and two females, all of whom were involved in a sign language training program and were easily handled. The adolescent group included three males and one female who were housed together in a single cage. All the adolescents had previously been accustomed to close human contact and had participated in varying amounts of sign language training. One of the adolescents, Booee, had been subjected to surgical severance of the corpus callosum and the optic chiasm as an infant, making him a particularly interesting subject for this study. Subjects were pretested to determine hand preference in a series of tasks involving opening box lids and reaching for food items. Half the juveniles and half the adolescents revealed right hand preferences, and the remaining subjects revealed left hand preferences. All subjects used the preferred hand on approximately 75% of trials on the particular tasks tested. Procedure

With the juvenile subjects (who were easily handled) the experimenter sat or stood directly in front of the subject and established eye contact, usually by vocally addressing the chimpanzee. When the subject broke eye contact and the eyes shifted momentarily to one direction and returned immediately to the experimenter, without fixating on another object, the experimenter recorded the direction of the eye movement. The juveniles were tested individually in blocks of six trials, with experimenters alternating on every block of trials. This procedure could not be duplicated for the adolescents, since they could not be removed from their cage. They could not be tested individually, nor could the experimenters be systematically rotated, since the older chimpanzees could not be forced to attend to any particular experimenter on demand. All the adolescents were observed by three experimenters, but the subjects determined which experimenter would observe them at any given moment. The experimenters spaced themselves around the adolescents’ cage, and when a chimpanzee initiated interaction with one of them, that experimenter would record CLEMs until the chimpanzee moved away. Forty-eight observations were made for each subject on at least two non-consecutive days spanning a period of at least a week. Since the subjects were so easily distracted, only one experimenter at a time could observe eye movements, making assessment of inter-observer reliability impossible. Analysis of the eye movement data from the juvenile group, however, demonstrated that all experimenters reported comparable proportions of left and right eye movements for all subjects.

RESULTS The direction of CLEMs after a break in eye contact was recorded for each subject. Occasionally, a subject’s eyes would move upward or downward instead of laterally; these trials were recorded, but were eliminated from the determination of probability scores found in Table 1. Percentages and exact cumulative binomial probabilities for the preferred direction of CLEMs out of all lateral eye movements were determined using a probability value of 0.50 for right and left eye movements (see Table 1). Table 1. Exact cumulative binomial probability and precentage of eye movements Subject Juveniles

Kelly Onan Vanessa Mac

Age (yr, month) 4.11 5.2 5.5 5.10

Adolescents

Bruno Booeet Pancho Washoe

9.10 10.10 12.3 12.4

n = Y= R = L = * =

Hand preference R R L L

n 47 46 46 41

24 24 28 22

L R L R

48 48 48 48

29 (L) 26 (L) 33 (L) 36 (L)

r (R) (L) (R) (R)

E(n,r,P = 0.50) 0.50000 0.44150 0.09196 0.33761 0.09671 0.33273 0.00664’ 0.00036*

% 51 53 61 54 60 54 69 75

number of trials resulting in a conjugate lateral eye movement (CLEM). the greater of the number of right or the number of left CLEMs. right. left.

P
subject.

The juvenile subjects showed no bias to one direction or the other, although the cumulative binomial probability for the frequency of right CLEMs for Vanessa was less than 0.10. Among the adolescents, both Pancho and Washoe (the two oldest) showed cumulative binomial probabilities of less than 0.01 for left

NOTE

761

CLEMs. and Bruno’s probability score ~vas less than 0.10 for ieft CLEMs. Booee, the “split brain” subject, showed no significant difference in frequency of left and right CLEMs. DISCUSSIOh’ The results lend credence to the notion that the preferential activation of the human cerebral hemispheres may be closely approximated in chimpanzees. The eye movement data show a rather orderly increase in the consistency of direction of CLEMs with increasing age - with the exception of the two subjects Mac and Boo-e. Booee’s data is not surprising, given the fact that his brain has been split from infancy. The data from Mac might reflect an overall I-etardation in this subject’s development. Mac, the oldest of the juvenile group, is also the smallest in terms of height and weight: furthermore, he exhibits behavior patterns which are immature for a male of his age. Clearly. a much more extensive study with a larger subject pool covering a wider age range is indicated, such that maturational factors in the development of consistent), in direction of CLEMs might be more conclusively determined. This preliminary study suggests that this is a promising area for further research; however. an extensive study of CLEMs in this species will require some methodological innovation. The subjects of the present study were appreciative of human attention, so that establishing eye contact with them and observing breaks in eye contact were relatively easy tasks. The recording of eye movements in a population that might include less tractable subjects, however, would require recording techniques that do not involve close interaction with the subjects-techniques which could be validated by several observers. The filming techniques employed with human subjects would present problems. since the chimpanzee eye does not have a white sclera, making assessment of eye movements from a filmed image extremely difficult. Thus, the methodological challenge seems basic to future studies of this nature. Once this challenge is met, the comparison of chimpanzees with and without language training might provide new insight into the basis of hemispheric activation biases and into the neural organization of language behavior.

REFERENCES 1. GESELL.A. and AMES, L. B. The development of handedness. J. gcner. Psychol. 70, 155-175, 1947. 2. BELMONT.L. and BIRCH. H. G. Lateral dominance and riaht-left awareness in normal children. Child Develop. 34(2), 257-270,‘1963. 3. SINCWIR, C. Dominance patterns of young children-follow-up study. Percept. Mot. Skills 32(l), 142, 1971. 4. HARDYCK,C. and PETRINOMCH,L. F. Left-handedness. Psychol. Bull. 84(3), 385-404,1977. 5. GAZZANIGA,M. S., BOGEN,J. E. and SPERRY,R. W. Some functional effects of sectioning the cerebral commisure in man. Proc. narn. Acad. Sci.. U.S.A. 48,1965, 1962. 6. SPERRY,R. W. Hemisphere disconnection and unity in conscious awareness. Am. Psychol. 23, 723-733, 1968. 7. GARDNER,R. A. and GARDNER, B. T. Teaching sign language to a chimpanzee. Science, N.Y. 165, 664-672, 1969. 8. PREMACK,D. Language in a chimpanzee? Science, N.Y. 172, 808-822, 1971. 9. FOUTS, R. S. Acquisition and testing of gestural signs in four young chimpanzees. Science. N.Y. 180, 978-980, 1973. 10. RU~.LBAUGH, D., GILL, T. V. and VONGLASERSFELD, E. C. Reading and sentence completion by a chimpanzee (Pan). Science, N.Y. 182,731-733, 1973. II. YENI-KOMSHIAN,G. H. and BENSON,D. A. Anatomical study of cerebral asymmetry in the temporal lobe of humans, chimpanzees, and rhesus monkeys. Science, N.Y. 192,387-389,1976. 12. DEWSON,J. H., III Preliminary evidence of hemispheric asymmetry of auditory function in monkeys. In Laterolizafion in fhe Nervous System, S. HARNARD, R. W. Don, J. JAYNES,L. GOLDSTEIF;and G. CRAUTHAMER(Editors), pp. 63-71. Academic Press, New York, 1977. 13. FINCH, G. Chimpanzee handedness. Science. N. Y. 94,117-l 18,194l. 14. CHORAZYNA,H. Shifts in laterality in a baby chimpanzee. Neuropsychologia 14,381-384,1976. 15. F&FIELD, W. and ROBERTS,L. Speech ond Bruin Mechanisms. Princeton University Press, Princeton, 1959. 16. DAY, M. E. An eye-movement phenomenon relating to attention. thought, and anxiety. Percept. Mot. Skills 19.44346, 1964. 17. DUKE. J. Lateral eye-movement behavior. J. gen. Psychol. 78, 189-195, 1968. 18. BAKAN,P. The eyes have it. Psychol. Today4.64-69.1971. 19. GUR. R. Conjugate lateral eye movements as an index of hemispheric activation. J. Pers. Ser. Psycho!. 85, 322-124,

1976.

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Deutschsprachige Zusammenfassung: Bei vier juvenilen und vier adoleszonten Schimpansen (Pan troglotydes) wurde die Richtung konjugierter horizontaler Blickbewegung fcstgestellt und bewertet. Bei zwei llteren adoleszenten Schimpansen wurde eine signifikante Neigung zugunsten von Blickbewegungen nach links gefunden. Weder die beiden jiingerenadoleszenten noch die vier juvenilen Schimpansen zeigten eine signifikante Asymmetrie in Bezug auf die Richtung konjuziorter hcrizontaler Blickbewegungen. Die Daten sprechen dafiir,daR 3ltere Vcrtreter dieser Spezies, die dem Menschen so nah verwandt sind, eine Neigung zu einzelhemisphsrischer AktivitBt zeigen, die #hnlich derjenigen ist, die der iiomosapiens aufweist.