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Intern. J . Neuroscience, 1992, Vol. 65, pp. 29-36

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THE RELATIONSHIP BETWEEN LEFTWARD TURNING BIAS AND VISUOSPATIAL ABILITY IN HUMANS HAROLD W. GORDON and ELIZABETH C. BUSDIECKER University of Pittsburgh, Pittsburgh, PA

H. STEFAN BRACHA VA Medical Center, North Little Rock, AR (Received October 28, 1991)

A significant relationship was found between a bias to make complete counter-clockwise (leftward) turns and performance levels on tests of visuospatial function. Subjects who turned preferentially to the left over a four-day period performed above average on visuospatial tests with those having the greatest turning bias performing the best. Subjects who tended to turn to the right performed below average on tests of visuospatial function. There was no relationship between rotational bias and verbosequential skills, but there was a significant relationship between turning bias and a cognitive profile defined as the difference between visuospatial ability and verbosequential ability. The cognitive profile effectively partialed out overall ability suggesting that the turning bias is related to the bias for better visuospatial processing rather than the level of visuospatial performance per se. Asymmetric turning has been shown to be related to asymmetries of dopamine activity in rats. Therefore, the present results are discussed in relation to the possibility that the dopamine neurotransmitter system may underlie both rotational behavior and visuospatial cognitive function in humans. Keywords: Rotation, turning bias, laterality, hemisphericiq, visuospatial abiliw, dopamine.

Rotational asymmetry is the tendency to turn spontaneously in circles preferentially either toward the left or right side. In rats it has been demonstrated that this asymmetry was related to an asymmetry of dopamine concentration in the striatal area [Zimmerberg, Glick, and Jerussi, 19741. The side containing more dopamine was contralateral to the preferred direction of rotation. A number of studies have since substantiated the asymmetrical dopamine activity/preferential turning relationship. For example, a pre-existing turning asymmetry was significantly enhanced with dopamine agonists such as amphetamine [Click and Cox, 19781 and cocaine [Click, Hinds, and Shapiro, 19831. In contrast, dopamine antagonists such as chlorpromazine have the effect of blocking these rotational behaviors [Crow and Gillbe, 19731. Strong rotational preferences have also been shown to exist in certain human groups and support the asymmetrical dopamine theory. Rotational asymmetry favoring counterclockwise (leftward) turning has been observed in one study with ten male schizophrenic patients [Bracha, 19871. This finding supports the widely held notion that dopamine is involved in the etiology of schizophrenia and that the right cerebral hemisphere is more intact than the left. The tendency toward leftward turning in the schizophrenic patients contrasts with a control group of hospital employees who on Correspondence to: Harold W. Gordon, Ph.D., National Institute of Drug Abuse, Rockwall 11-Suite 615, 5600 Fishers Lane, Rockville, MD 20857 This work was carried out with support from the University of Pittsburgh Honors College

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H.W. GORDON, E.C. BUSDIECKER AND H.S. BRACHA

the average favored no specific direction. Half turned toward the left; the other half favored the right. In another study, patients with right-sided hemi-Parkinson’s disease, showed a strong rotational preference to the left [Bracha, Shults, Glick, and Kleinman, 19871. Because patients with right-sided symptoms have more substantial damage in the area of the lefi substantia nigra, the observed turning behavior was, in effect, away from the side of the higher (i.e., normal) dopamine activity. There was one patient in the study who showed left-sided Parkinsonian symptoms and who rotated preferentially to the right. In a third study, 23 right-handed, male patients with stroke-induced frontal and parietal lesions turned away from the side of the damaged hemisphere [Bracha, Lyden, and Khansarinia, 19891. While this seems to contradict conventional wisdom, studies of unilateral lesions in the striatal area of rats show that the immediate postlesion effect of circling toward the side of the lesion later reverses itself. It is believed that after 15-30 days, the number of dopamine receptors increases, thereby causing a dopaminergic “supersensitivity” [Glick and Cox, 19781. This explanation seems even more reasonable since it was secondarily observed in the lesioned patients that the turning bias increased with age of lesion. This suggests that there is a continued enhancement of dopaminergic activity at the lesion site. These pathological cases highlight an induced asymmetry of dopaminergic activity. But little has been said of the control group which also had rotational preferences [Bracha, Seitz, Oteman, and Glick, 19871. In this group, the distribution of individual turning biases was normal with a mean of zero, suggesting that the subjects, as a group, had no preference for any one direction. Equal numbers of them had turning biases either to the right or the left; some subjects had strong left or right turning preferences. The question is whether these turning differences in normal humans are also based on asymmetries of dopaminergic activity as they are in animals, and appear to be in patients with schizophrenia and hemi-Parkinson’s disease. If so, it would be of further interest to determine whether or not these rotational preferences are related to any of the other well-known lateral asymmetries of hand skill, or attentional asymmetries such as those assessed by dichotic listening. In addition, it may also be true that the rotational asymmetries are related to lateralization of cognitive abilities associated with the left and right cerebral hemispheres. These relationships can be determined by measuring the turning tendency in free-moving, healthy humans and comparing this tendency to asymmetries in performance on cognitive tasks.

METHODS Subjects

Nine female and five male subjects between the ages of 18 and 35 were recruited from university classes. Handedness was not a selection criterion, but all subjects preferred their right hand for more than half of an 8-item inventory [modified from Briggs and Nebes, 19751. All subjects were nonsmokers and nonusers of medications or abusers of drugs according to self-report. In addition, all subjects who used caffeine were asked to abstain during their participation in the study; heavy caffeine users were excluded from the study.

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Apparatus and Tests Rotation Rotation was measured by an electronic device developed by one of us (HSB) and used and described elsewhere [Bracha, 19871. Briefly, it is small, 6 cm x 13 cm X 4 cm (about the size of a hand-held calculator), and light, weighing less than a kilogram, so that it can be worn unobtrusively on a belt. Rotation was measured by sensors associated with a compass oriented to magnetic North. It was calibrated to produce a count when a subject turns 90, 180, or 360” in one direction without turning back. The turns are counted and stored, and can be read on a digital display. Each subject wore the device for a period of four consecutive days or until at least 350 full (360”)turns (right and left combined) were recorded. Each four-day period included one weekend day in order to get a good representation of a subject’s complete free-moving routine. Of course, there are several ritualistic turns that all subjects would make, but it is expected that these would tend to cancel each other out. For example, one usually returns home from work along the same path but with reversed turns from the path traveled to work. The “meaningful” turns would be those unstructured turns performed, for example, by a subject’s pacing while waiting for an elevator. Subjects participated only after reading and signing an informed consent form. They were encouraged to ask questions, and the experimenter gave a description of the general experimental procedure. However, they were only told that the electronic device measured “activity“ and not that it specifically measured rotation. Each subject was also instructed to wear the device all day, removing it only for sports, showers, sleep, etc. Each subject kept a diary to record the times the device was removed. An experimenter met with each subject once a day to record the number of turns, and to insure compliance. Cognitive performance: hand performance Hand performance was assessed by a peg-moving task that has been regularly used in several studies on thousands of subjects [Annett, 19851. The task required the subject to move ten pegs (5 cm long and 1 cm diam) from one set of holes to a matched set of holes 20 cm away as quickly as possible. This task was performed six times with each hand, starting with the dominant hand. The experimenter reported the reponse time after each trial, and provided constant encouragement to improve the response time in each subsequent trial. The performance of the best five trials was averaged for each hand. A laterality index was calculated by taking the difference in the average times between the hands and dividing by the total for the two hands. Divided attention was assessed by a standard test of dichotic listening [Gordon, 19801. Forty-eight sets of digits were played to the left and right ears. For each trial there were three pairs of digits played simultaneously, one pair at a time at the rate of two pair per second. The subject was required to write as many digits from both ears (free recall) as possible. A laterality index was calculated from the difference between the ear scores divided by the overall performance. Cognitive asymmetry was assessed by specialized tests of cognitive function that have been selected to assess verbosequential ability (associated with the left hemisphere) and visuospatial ability (associated with the right hemisphere) [Gordon, 19861. The validity of the choices of the verbosequential and visuospatial tests has been demonstrated in factor analyses in numerous studies. There are eight tests in the battery loading consistently on one of two factors and accounting for more than 50% of the variance. These factors are stable across age groups from children to adults

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H.W. GORDON, E.C. BUSDIECKER AND H.S. BRACHA

and between both sexes [Gordon and Kravetz, 19911. Norms are available so that they can be combined on these factors in a composite visuospatial score and a composite verbosequential score, or a cognitive profile (of performance asymmetry) obtained by subtracting the visuospatial score from the verbosequential score. Separate norms are used for males and females. Verbosequential functions are assessed by tests of perception and memory of sequences of familiar sounds and of numbers (Serial Sounds and Serial Numbers). Verbal skills are assessed by written tests of word production (fluency) (Word Production, Letters and Word Production, Categories). In the Serial Sounds test, sequences of two to seven familiar sounds (e.g., baby, horse, bell, etc) are presented at the rate of one sound per two seconds by an audio cassette tape. The subject’s task is to recall the sequence by writing the names of the sounds in the correct serial order. In the Serial Numbers task, the subjects hear sequences of two to nine digits in length, presented at the rate of one per second. The subject’s task is to write the numbers in correct serial order. For both tests the score depends on how many items are recalled in correct sequences even if the whole sequence is not correct. In Word Production, Letters, subjects write as many words as possible in one minute that begin with a given letter of the alphabet (C, L, and F). The score is the total number of words listed for all three letters. In Word Production, Categories, subjects write words that fit into broad categories (Animals and Food). The score is the total number of words for both categories. Visuospatial function is assessed by a test of locating points in two dimensional space (Localization), a test of mental rotation (Orientation), a test of perception in three dimensions (Touching Blocks), and a test of perceptual closure (Form Completion). In the Localization test, the subject sees an “x” marked in a frame on a projection screen and must place an “x” on an answer sheet in the same location. The Orientation test was adapted from stacks of cube stimuli [Shepard and Metzler, 19731. The subject must determine which two of three similar geometric configurations are the same, except for their spatial rotation. In the Touching Blocks test the subject is required to determine how many blocks are touching a designated block in a stack of seven to ten blocks. The stimulus objects were adapted from [MacQuarrie, 19561. Finally, the Form Completion requires identification of incomplete silhouette figures [French, Ekstrom, and Price, 1973; Thurstone and Jeffrey, 19661. The Symbol Digit Modalities Test [Smith, 19731 was given to assess a general performance level. This test has been used in previous studies with the visuospatial and verbosequential cognitive tests as a covariate because it factor loads about equally on both cognitive factors. In the test, there are nine symbols that correspond to the digits 1 to 9 in a response key. The subject’s task is to fill these digits in blank boxes beneath a series of the symbols. The score is the number of boxes correctly filled in 90 seconds. RESULTS Specific Cognitive Function

There was a significant correlation ( r = .68; p < . O l ) between the preference for turning counter-clockwise and performance on tests of visuospatial function. The relationship held only for complete turns (360” or more); 90” and 180” preferences did not significantly correlate. This means that subjects who made relatively more complete counter-clockwise (leftward) turns performed higher on tests of visuospatial skills than those who favored clockwise turns. (See Figure 1 .) There were four sub-

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TURNING BIAS AND VISUOSPATIAL ABILITY

2.c Int J Neurosci Downloaded from informahealthcare.com by Universitaets- und Landesbibliothek Duesseldorf on 10/24/13 For personal use only.

0

1.c-

0. 0 0 0

0 0

0.c-

- 1.c-2. -0.4 Leftward

0

0

I

-0.2

I *

0.0

TURNS

I

0.2

0.4 Rightward

(Normalized) FIGURE 1 Visuospatial ability as a function of turning bias. Visuospatial ability is a composite of standard scores from four tests (see text). Turning bias is the difference between right and left turns divided by the total number of turns.

jects who turned more times to the right: three of those four received scores below the norm on the visuospatial tests. All ten remaining leftward turners had scores at or above the norm on visuospatial tests. When the scores on the Symbol Digit Modalities Test were used to covary for performance level, the partial correlation improved slightly (r’ = .72). There was no correlation between performance on verbosequential skills and turning preference. However, there was a correlation ( r = . 6 3 ; p < .02) between leftward turning and the cognitive profile, defined as the difference between the visuospatial and verbosequential scores. By stepwise multiple regression it was determined that the best prediction of turning preference included both the visuospatial and the cognitive profile, accounting for more than 55% of the adjusted variance. The partial correlation of each predictor was significant ( p < .05) suggesting that leftward turning is related not only to performance on visuospatial skills with the cognitive profile held constant, but also turning is related to the cognitive profile when performance on visuospatial skills is controlled. Finally, it should be noted that leftward turning preference is positively correlated with three of the four subtests (with a trend for the fourth) that made up the visuospatial composite: Localization, r = .60, p < .05; Orientation, r = .63, p < .02; Touching Blocks, r = .75, p < .01; Form Completion, r = .46, p < . l o . Although sex-related norms were used in this study to correct for sex differences in this sample, the tests producing the strongest results were Orientation and Touching Blocks which have been shown to be better performed by right handed males and left handed females [Gordon and Kravetz, 19911. Laterality Measures

Neither the asymmetry of hand performance assessed by the peg-moving task nor the asymmetry of divided attention assessed by the dichotic listening tasks was correlated with turning preference. Furthermore, these tasks were not correlated with

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H.W. GORDON, E.C. BUSDIECKER AND H.S. BRACHA TABLE 1 Pearson Correlations between Rotation, Cognitive Function, and Lateral Asymmetries

Variables Normalized rotation (L - W/(L + R) 2. Visuospatial skill 3 . Verbosequential skill 4. Cognitive profile (Vis - Ver) 5 . Hand asymmetry fR - L)/(R + L) 6 . Ear asymmetry (R + L)

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1.

1

2

3

4

5

.677* ,172

.630* .282

-.I92

.689* ,374 - ,047

,035

- .414

-

203

-.319

-

-065

- ,040

- ,419

cognitive performance. There was only a slight trend for the asymmetry of the pegmoving task to be related to the ear asymmetry. (See Table 1 . )

DISCUSSION Performance on tests of visuospatial ability was significantly correlated with the degree of bias toward complete counter-clockwise (leftward) turning. Similarly, there was also a correlation between the leftward bias and the degree of superior performance on visuospatial skills over verbosequential skills. While additional subjects are needed to insure the robustness (and improve the power) of this observation, the significant correlation was driven by a fairly uniform distribution of data. Since no underlying neural systems were studied directly, we can only speculate as to the cause of this correlation. The most parsimonious assumption is that dopaminergic activity which has been found to be responsible for rotational behavior observed in the original studies of rats and in subsequent studies in patients with various brain disorders is likewise responsible for the rotational behavior that we observed in normal subjects. This assumption would be easily tested in double-blind, crossover studies in which dopamine agonists and antagonists are compared to placebo in normal subjects moving freely in a directionally unbiased environment. We were careful to eliminate external sources of chemical enhancements in our subjects in order to provide a baseline for future studies. The relationship of leftward turning to visuospatial ability and to the cognitive profile (and not to the verbosequential performance or laterality bias) is more obscure and requires additional assumptions. First, there must be an assumption that the relationship is related to the same underlying dopaminergic mechanisms associated with turning biases. Accordingly, if the rotational behavior is related to dopaminergic activity, one conclusion would be that visuospatial function is also related to the dopamine system. This could be tested in the same study design as outlined for rotational behavior in humans. The traditional neuropsychological concept that anatomical substrates are responsible for visuospatial function poses a challenge to acceptance of this new idea that the dopamine system may underlie visuospatial function (i.e., performance ability on spatial tasks). However, the concept of a neurotransmitter system as the basis of visuospatial function is attractive because it resolves many of the failures to find

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TURNING BIAS AND VISUOSPATIAL ABILITY

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relationships between lateral dominance and cognitive performance [Boles, 19911. The emphasis of a neurochemical basis of specialized (visuospatial) cognitive function is also consistent with other evidence of shifts in cognitive performance. In studies using visuospatial and verbosequential tests similar to those used here, it was found that performance o n visuospatial skills was better when subjects were awakened from Rapid Eye Movement (REM) sleep than when they were awakened from Non-REM sleep [Gordon, Frooman, and Lavie, 1982; Lavie, Metanya, and Yehuda, 19841. Performance on verbosequential tests showed the reverse effect. Because neurotransmitters can fluctuate at the 90-minute intervals between REM and Non-REM sleep, and anatomical substrates obviously do not, these findings suggested that there was a neurochemical component for both types of cognitive functions studied. There is also evidence that these fluctuations in cognitive performance occur in the waking period due to ultradian rhythms of performance levels in these cognitive skills [Gordon and Stoffer, 1989; Gordon, Lee, and Stoffer, 1990; Klein and Armitage, 19791. Finally, there are several indications of relationships between hormonal levels and performance on cognitive tasks both across and within subjects [Gordon and Lee, 1987; Gordon, Corbin, and Lee, 1987; Hampson, 19901. While the strength of the relationship between hormone activity and the dopaminergic system is yet to be determined, these data are presented as evidence of an underlying neurochemical component for performance on cognitive tests. If measurement of rotational behavior in humans can be established as a paradigm for assessing asymmetries of dopaminergic activity, a program of research into the relationship between cognitive function and dopamine can be established.

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Gordon, H. W., & Lee, P. (1986). A relationship between gonadotropins and visuospatial function. Neuropsychologia, 2 4 , 563-576. Gordon, H. W., & Stoffer, D. W. (1989). Ultradian rhythms of right and left hemisphere function. International Journal of Neuroscience, 47, 57-65. Gordon, H. W. (1980). Cerebral organization in bilinguals: I. Lateralization. Brain and Language, 9 , 255-268. Gordon, H. W. (1986). The Cognitive Laterality Battery: Tests of specialized cognitive function. I n ternational Journal of Neuroscience, 29, 223-244. Gordon, H. W., Corbin, E. D., & Lee, P. A. (1986). Changes in specialized cognitive function following changes in hormone levels. Cortex, 2 2 , 399-415. Gordon, H. W., Frooman, B., & Lavie, P. (1982). Shift in cognitive asymmetries between wakings from REM and NREM sleep, Neuropsychologia, 2 0 , 99-103. Gordon, H. W., Lee, P. A., & Stoffer, D. S. (1990). Ultradian rhythms in specialized cognitive function. Journal of Clinical and Experimental Neuropsychology, 1 2 , 40. Hampson, E. (1990). Variations in sex-related cognitive abilities across the menstrual cycle. Brain nnd Cognition, 1 4 , 26-43. Klein, R., & Armitage, R. (1979). Rhythms in human performance: 1 1/2-hour oscillations in cognitive style. Science, 2 0 4 , 1326-1327. Lavie, P., Metanya, Y., & Yehuda, S. (1984). Cognitive asymmetries after wakings from REM and NONREM sleep in right-handed females. Internationaf Journal of Neuroscience, 23, 111-1 16. MacQuarrie, T. W. (1953). MacQuarrie Test f o r Mechanical Ability. Monterey, CA: California Test Bureau. Shepard, B. M., & Metzler, J. (1971). Mental rotation of three-dimensional objects. Science, 171, 701703. Smith, A. (1973). Symbol-Digit Modalities Test. Los Angeles, CA: Western Psychological Services. Thurstone, L. L., & Jeffrey, T . E. (1966). Closure speed. Chicago, IL: Industrial Relations Center. Zimmerberg, Z., Glick, S. D., & Jerussi, T. P. (1974). Neurochemical correlate of a spatial preference in rats. Science, 185, 623-625.

The relationship between leftward turning bias and visuospatial ability in humans.

A significant relationship was found between a bias to make complete counter-clockwise (leftward) turns and performance levels on tests of visuospatia...
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