Measurement of Spontaneous Rotational Movement (Circling) in Normal Children Sidney M. Gospe Jr, MD, PhD; Bernardo J. Mora; Stanley D. Glick, PhD, MD Abstract

asymmetry of basal ganglia dopaminergic function has been demonstrated in rats and related to both spontaneous and drug-induced rotation. An electronic device that measures the same kind of rotational movements in humans has been developed, and we have utilized this "rotometer" to study spontaneous rotational movement in prepubertal children. There was no significant difference between boys and girls in their average rate of rotation; however, left hemispheredominant boys were stronger rotators than left hemisphere-dominant girls. Both boys and girls made significantly more full turns to the left than to the right. These findings did not vary with age. Our observations are strikingly different from those obtained in previous studies of normal adults, in which women were stronger rotators than men, left hemisphere-dominant women turned to the left, and left hemisphere-dominant men rotated to the right. This study suggests that maturational changes in rotational behavior must occur, perhaps progressing to the adult pattern during puberty. The rotometer used in this study may provide useful information regarding the status of the basal ganglia in children with specific neurobehavioral conditions such as attention deficit disorder and Tourette’s syndrome. ( 1990;5:31-34). J Child Neurol An

Laboratory investigation

over

the past several

imbalance of hemiin basal ganglia is the spheric dopaminergic activity correlated with circling behavior (rotation) in animals.l2 Circling movements were first studied in animals after creating a hemispheric dopamine imbalance with unilateral electrical stimulation or lesions, and subsequently, an endogenous dopaminergic asymmetry was noted and related to both druginduced and spontaneous circling.’,’ Asymmetry of dopamine levels in postmortem human globus pallidus has been measured,’ and recently, spontaneous circling in normal adult men and women has been documented.6 The latter study showed that men and women rotated preferentially to the left or right during a routine day and that women were stronger

years has shown that

an

Received Nov 29, 1988. Accepted for publication Jan 20, 1989. From the Departments of Neurology, Pediatrics, and Pharmacology & Toxicology, Albany Medical College, Albany, NY; and the Departments of Neurology and Pediatrics, School of Medicine, University of California Davis, Davis, CA. This research was presented at the 17th Annual Meeting of the Child Neurology Society, Halifax, Nova Scotia, September, 1988. Address correspondence to Dr Sidney M. Gospe, Jr, Department of Neurology, University of California, Davis Medical Center, 2315 Stockton Boulevard, Sacramento, CA 95817.

rotators than men. A subsequent study of individuals with hemi-Parkinson’s disease showed that these patients rotated toward the hemisphere con7 taining less striatal dopaminergic activity / Several neurologic and neurobehavioral syndromes of childhood including attention deficit disorder and Tourette’s syndrome are believed to be due, in part, to dysfunction of dopaminergic systems. Studies of circling behavior in children affected with these conditions may complement other clinical descriptions of these disorders and may also assist in guiding pharmacologic therapy. Before rotation in these patients can be evaluated, circling behavior in normal children needs to be assessed. This study was designed to record spontaneous rotational movements in prepubertal children.

Subjects and Methods The human &dquo;rotometer&dquo; used to record rotation in normal adults’ and patients with hemi-ParkinsoniSM7 was utilized in this study. The rotometer is a small, lightweight, rechargeable device that the subject wears in a belt-mounted calculator case. The device consists of two functional components : the position sensor and the electronic processing circuit. The position sensor monitors changes in the orientation of the dorsal-ventral axis of the subject. Magnetic north is used as an external reference and a compass is used

31

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to track this reference. A compass transducer system moves with the subject relative to the needle. A microchip is programmed with algorithms for generating left and right full (360°) turns as well as left and right quarter- (90°) turns. If a subject enters four quadrants sequentially in the same direction (ie, moves 360°), a full turn (as well as four quarterturns) is counted for the respective direction. If, however, a subject enters three quadrants sequentially in the same direction but then enters a quadrant from the opposite direction of the previous move, a new direction is begun and only quarter-turns are counted. The resulting output is determined by precisely the same logic employed with an analogous apparatus commonly used for rodents.5,8 Several rotational indices were calculated from these data. Net rotation and percent preference were used as indices of asymmetry: net rotation refers to the absolute difference between full turns in the preferred and nonpreferred directions; percent preference refers to the percentage of full turns in the preferred direction. Extra quarter-turns, a measure of nonlateralized activity,9 refers to the result of subtracting four times the number of full turns from the number of quarter-turns. The subjects were 56 children between the ages of 6 and 9 years. Subjects were recruited through a variety of pediatric practices and through the staff of the Albany Medical Center. The study population included 30 girls (mean age ± SD, 7.88 ± 1.17 years) and 26 boys (mean age, 7.88 ± 0.97 years). Prior to study, the children were screened for neurobehavioral and developmental conditions, and informed consent was obtained from the parent of each subject. Each child’s hand, foot, and eye preference were determined by using a lateral dominance examination modified from the laterality scale of the Halstead-Reitan battery Twelve girls and 13 boys were right-hand, right-foot, and right-eye dominant, ie, left-hemisphere dominant as defined by Reitan.’° Sixteen girls and 12 boys manifested left-hand and/or left-foot and/or left-eye dominance and constituted the mixed dominance group. Dominance in two girls and one boy could not be determined. The subjects were studied during the 1987 summer vacation and they were all evaluated in their homes. Each subject wore the rotometer for four hours and their activities were not restricted. Each child was completely unaware of the purpose of the study and of the type of information being recorded by the device. This study was approved by the Human Studies Committee of the Albany Medical

College.

TABLE 1

Rotational Indices in Boys and Girls

* mean ± SD. XQT extra quarter-turns. =

indices decreased. However, a two-way analysis of variance (ANOVA) for sex and age (6, 7, 8, and 9 years) demonstrated that none of these changes were

significant. The distribution between left and right full turns for all subjects (Table 2). Strikingly, a left-turning bias was noted in both sexes. Twentyfour girls (80%) and 20 boys (77%) rotated preferentially to the left. To determine whether a relationship between direction preference and the various rotational indices was present, a two-way ANOVA for sex and preferred direction was performed. A significant direction effect was present for both net rotation was uneven

and

percent preference (Table 3).

When comparing hemispheric dominance with the direction of preferred turns, the left-turning bias was significant in left-hemisphere dominant boys (P - .0005, x2 7.69) and in left-hemisphere dominant =

girls (P .041, x2 4.08). Two-way ANOVA (sex and dominance) of the rotational indices revealed a significant sex-dominance interaction (P .022, F 5.49) for net rotation (Table 4). The basis for this =

=

=

=

TABLE 2 Distribution of Subjects With Respect to Preferred Direction of Rotation, Sex, and Dominance

Results All

subjects made numerous spontaneous full turns during the test session. The range (left plus right 360° turns) was 51 to 783 in girls and 67 to 797 in boys. On average, boys made more total full turns than girls; however, the difference was not significant. Table 1 shows that boys also had more full turns in both the preferred direction and the nonpreferred direction than girls, as well as higher net rotation, percent preference, and extra quarter-turns. However, none of these differences were significant. As age increased from 6 to 9 years, the values for all of the rotational

*

t

Significant left bias in left hemisphere-dominant boys (P

=

.005,

Significant left bias

=

.041,

X’=7.69).

in left

xZ = 4.08).

32

Downloaded from jcn.sagepub.com at University of Otago Library on March 13, 2015

hemisphere-dominant girls (P

TABLE 3 Rotational Indices in Girls

Left-Turning Preference and Right-Turning Preference Boys and

* Mean ± SD. t ANOVA significant direction effect t ANOVA significant direction effect

XQT

=

extra

(P (P

=

=

.026, F .002, F

=

=

5.18). 10.04).

quarter-turns.

TABLE 4 Rotational Indices in Left Hemisphere-Dominant and Mixed Dominance

Boys and Girls

* Mean ± SD. ANOVA significant sex-hemisphere interaction (P = .022, F 5.49); left hemisphere-dominant boys significantly different from left hemisphere-dominant girls (P .016, t test).

t

=

=

XQT =

interaction

was

extra

that left

quarter-turns.

hemisphere-dominant boys rotators than left hemi-

significantly stronger sphere-dominant girls (P .016, t test).

were

=

bias also noted. right foot-domi-

Associations between direction of

and hand, foot,

turning

eye preference Right-handed (P = .021, x2 = 6.26) nant (P .008, x2 = 7.04) and right eye-dominant (P .005, x2 = 7.69) boys all had a left turning bias as did right-handed (P = .004, x2 = 8.04), right footdominant (P .016, x2 5.76) and right eye-dominant (P .009, X2 = 6.67) girls. There were no between left hand, foot, or associations significant and turning bias. eye preference were

or

=

=

=

=

=

Discussion The data from this study indicate that without being aware of it, normal prepubertal children rotate preferentially to the left or to the right while involved in routine daily activities. We have shown that the human rotometer that has been used to measure circling in both normal adults6 and patients with

hemiparkinsonism’

record these moveour male subin a 4-hour had more than jects recording period seven times the nonlateralized activity (total extra quarter turns) of adult males studied during an 8- to 9-hour recording, whereas the girls had nearly four times greater nonlateralized activity than women.66 Besides this rather predictable increase in general activity, there were many features of rotation behavior in children that were strikingly different from those of normal adults. Most important were that the vast majority of children preferred to rotate to the left and that this left turning bias was significant in both left hemisphere-dominant boys and left hemispheredominant girls. Moreover, both indices of asymmetry (net rotation and percent preference) were significantly greater in the left-turning population, indicating that children who are strong rotators prefer to turn to the left. In normal adults, left hemispheredominant men rotate to the right; a left-turning bias is women present in both left hemisphere-dominant and mixed dominant men.66 can

reliably

ments in very active children.

Indeed,

33 Downloaded from jcn.sagepub.com at University of Otago Library on March 13, 2015

The significant sex differences in the rotational indices found in adults were not apparent in children. Whereas women were the stronger rotators and made more full turns in the preferred direction, there were no significant differences in these indices between boys and girls. The only significant sex difference in children was that left hemisphere-dominant boys were stronger rotators than left hemispheredominant t

girls (net rotation,

46.7

v

11.4, P

=

.016,

test).

Since the rotation behavior of adults and children is so different, a developmental maturation of this behavior must occur. Our study population ranged in age from 6 to 9 years, and there were no significant age-related differences in the rotational indices or turning biases. The maturation of rotation behavior to the adult pattern must therefore occur at an age greater than 9 years. A likely time for this maturation to occur would be during puberty, a time when maturation of neuroendocrine systems is also progressing. Although many important aspects of cerebral laterality have developed prior to puberty, eg, handedness and speech localization, it is reasonable to suggest that other neurobehavioral functions can continue to be modified during puberty.ll Clearly, further study of the developmental aspects of circling behavior is warranted. Once the development of rotation in normal children is documented, studies of circling behavior in young patients affected with such neurobehavioral disorders as Tourette’s syndrome and attention deficit disorder can be performed. Measurement of rotation in these patients may help characterize the role of the basal ganglia in these disorders, which are believed to be due, in part, to dysfunction of dopaminergic systems.

Acknowledgments This

study was supported Fellowship T35 HL 07506.

in

part by

NIH Summer Research

References SD, Jerussi TP, Fleisher LN: Turning in circles: The neuropharmacology of rotation. Life Sci 1976;18:889-896. 2. Pycock CJ: Turning behavior in animals. Neuroscience 1980;5: 1. Glick

461-514. 3. Glick SD, Shapiro RM: Functional and neurochemical mechanisms of cerebral lateralization in rats, in Glick SD (ed): Cerebral Lateralization in Nonhuman Species. Orlando, FL, Academic Press, 1985, pp 157-183. 4. Zimmerberg B, Glick SD, Jerussi TP: Neurochemical correlates of a spatial preference in rats. Science 1974;185:623-625. 5. Glick SD, Ross DA, Hough LB: Lateral asymmetry of neurotransmitters in human brain. Brain Res 1982;234:53-63. 6. Bracha HS, Seitz DJ, Otemaa J, Glick SD: Rotational movement (circling) in normal humans: Sex differences and relationship to hand, foot and eye preference. Brain Res 1987;411:231-235. 7. Bracha HS, Shults C, Glick SD, Kleinman JE: Spontaneous asymmetric circling behavior in hemi-Parkinsonism: A human equivalent of the lesioned-circling rodent behavior. Life Sci

1987;40:1127-1130. 8. Glick SD, Cox RD: Nocturnal rotation in normal rats: Correlation with amphetamine-induced rotation and effects of nigrostriatal lesions. Brain Res 1978;150:149-161. 9. Greenstein S, Glick SD: Improved automated apparatus for recording rotation (circling behavior) in rats or mice. Pharmacol Biochem Behav 1975;3:507-510. 10. Reitan RM: Manual for Administration of Neuropsychological Test Batteries for Adults and Children. Tuscon, AZ, Reitan Neuropsychology Laboratories, 1979, pp 70-74. 11. Geschwind N, Galaburda AM: Cerebral Lateralization. Cambridge, MA, MIT Press, 1987, pp 86-87.

Vignette right and proper that a strong interest be cultivated in a student of medicine in his senior years. Less just and good It is

From

Harry

Lee Parker: Clinical Studies in

Neurology,

1956.

is it that he be forced to swallow indigestible theory and dogma. The former principle he will remember forever after; the latter, at a later date, he will gleefully discard as the snake, wriggling with pleasure, gets rid of his own skin.

34 Downloaded from jcn.sagepub.com at University of Otago Library on March 13, 2015

Measurement of spontaneous rotational movement (circling) in normal children.

An asymmetry of basal ganglia dopaminergic function has been demonstrated in rats and related to both spontaneous and drug-induced rotation. An electr...
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