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Prevalent direction of reflective lateral eye movements and ear asymmetries in a dichotic test of musical chords

1994, Neuropsychologia

&wops~choloykr. Pergamon Vol 32. No 12. pp. 1515-1522. 1994 Elsevm Saence Ltd Punted in Great Brifam 002X-3932!94 $7.00+0 00 0028-3932(94)00092-l PREVALENT MOVEMENTS LATERALEYE DIRECTION OF REFLECTIVE TEST AND EAR ASYMMETRIES IN A DICHOTIC OF MUSICAL CHORDS P. SAN MARTINI,* Dipartimento di Psicologia, L. DE GENNARO, F. FILETTI, and C. VIOLANI C. LOMBARDOT di Psicologia, Universita di Roma “La Sapienza”, Roma, Italy; and tDipartimento Universita di Palermo, Palermo, Italy zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQ (Receioed 24 February 1994; accepted 2 July 1994) Abstract-Subjects who consistently move their gaze either to the right or to the left while reflecting on visuo-spatial or verbal questions are usually called “lateral eye movers”. This study evaluated auditory asymmetries to a dichotic test of musical chords in 23 right-handed females, selected through test-retest as reliable lateral eye movers; 12 were “left movers” (LMs) and 11 were “right movers” (RMs). During the assessment of the prevalent direction of gaze as well as during the dichotic test, the oculomotor activity was controlled through a video camera. The hypothesis was that the left ear advantage usually found with dichotic chords is enhanced in LMs and reduced in RMs, and that this effect is not due to the facilitating influence of lateral eye movements occurring during the task. Results show that: (a) left movers exhibit a marked advantage of the left ear while right movers do not exhibit any significant ear advantage; (b) despite the instruction to fix a central point, lateral movers tend to show unwarranted eye movements in their usual direction; (c) the effect of the prevalent direction of gaze on the dichotic advantage is not due to eye movements made during the dichotic test. These findings give further support to the hypothesis that the tendency to consistently shift the gaze to one side is related to hemispheric asymmetries as measured by lateralized tests. Key Words: lateral eye movements; dichotic test; musical chords; hemispheric asymmetry. INTRODUCTION It has been often reported that subjects, while reflecting on questions requiring visuo-spatial or verbal processing, tend to shift their gaze rightward or leftward according to the cognitive nature of the questions; further it has been hypothesised that these unintentional “reflective lateral eye movements” (RLEMs) might reflect a controlateral cerebral hemispheric activation (for reviews, see Refs [6,13, 181). Kinsbourne [22] proposed a neuropsychological model in which the activation produced by a cognitive task within one hemisphere tends to ‘overflow’ to the omolateral frontal eye fields (Brodman’s area 8), favouring RLEMs in the direction opposite to the activated hemisphere. It has been noticed, however, that about 25-35% of normal people show a reliable tendency to look either to the right or to the left, independent of the cognitive nature of the questions [13]. These subjects are usually called “right movers” (RMs) or “left movers” *Address for reprints: Pietro San Martini, dei Marsi 78, 00185 Roma, Italy. Dipartimento 1515 di Psicologia, Universita di Roma “La Sapienza”, Via 1516 zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA P. SAN MARTINI (‘I d (LMs). Bakan [2] has suggested that these individual differences in direction of gaze may reflect “easier triggering of activities in the hemisphere controlateral to the direction of eye movements”. This hypothesis does not clearly distinguish whether individual differences in usual direction of gaze are produced by a “preference” for cognitive strategies involving differentially one hemisphere or to a basic asymmetry in hemispheric activation, which does not necessarily imply differences in preferred cognitive strategies. As regards the first perspective, Bakan’s hypothesis has given rise in the last 20 years to many correlational studies which tried to find associations between prevalent direction of RLEMs and a host of cognitive and personality variables thought to be related to hemispheric functioning (for reviews, see Refs [6, 12, 13, 181). The results of these studies are highly inconsistent, most of the findings are weak, mixed, or even opposite to the hypothesis; only few studies yielding positive results have been successfully replicated [18]. Furthermore none of the measures used in these correlational studies is a direct and valid index of functional hemispheric asymmetry as defined by Beaumont, Young and McManus [3]. Relevant to the second perspective are the studies which have assessed whether prevalent direction of RLEMs is related to direct physiological measures of hemispheric activity (i.e. rCBF, PET, evoked potentials or EEG) or culid behavioural measures of hemispheric asymmetries, such as visual field and dichotic listening tasks. As regards the physiological measures, there is substantial evidence in favour of differences between right movers and left movers in resting hemispheric asymmetries as evaluated by EEG 12, 26, 361, by visual evoked potentials 14: Exp. 1, 331 and by rCBF [ 161, although some studies failed to find significant differences [4: Exp. 2, 5, 251. As regards the behavioural measures, three studies have been published using respectively a dichotic digit task 1271, a dichotic CV test [34] and a lateralized letter recognition visual task [lo]. Both the first and the second studies found a greater right ear advantage in right movers as compared to left movers; the last study showed only a trend in the hypothesised direction [t (37)= 1.14; P=O.13]. In the latter study the failure to find a significant relationship between prevalent direction of gaze and visual field asymmetry could be partially accounted for by the strong effect of visual asymmetry in the letter recognition task which might have left little variance for differentiating right and left movers. On the other hand, it is also possible that the positive result obtained by Nielsen and Sorensen [27] and by Struthers, Charlton and Bakan 1341 were entirely or partially due to a methodological artefact, that is to unwarranted oculomotor activity of the subjects during the task. In fact it has been shown that selective monitoring of one ear in the dichotic task is accompanied by a consistent pattern of directional eye movements characterised by big saccades and long changes of eye fixation in the direction of the relevant ear [14] and that oculomotor activity can affect asymmetry of performance for dichotic stimuli (e.g. 1191). Nielsen and Sorensen [27] did not provide any control for the oculomotor activity of their subjects during the presentation ofdichotic stimuli. Struthers, Charlton and Bakan [34], in a CV dichotic test, manipulated the direction of gaze, “by having subjects wear prismatic glasses which forced their gaze either 20’ to the left or to the right”, and did not actually check the ocular activity of their subjects; since prismatic glasses cause a ‘tonic’ lateral fixation, but not necessarily prevent occasional lateral shifts of the gaze, it is possible that on occasions lateral movers shifted the gaze in their usual direction. Aim ofthe present study was to evaluate auditory asymmetries to a dichotic test in a group of subjects selected as consistent lateral movers, providing a direct check of their oculomotor activity during the task. For this purpose we decided to use a dichotic test of musical LATERAL EYE MOVEMENTS AND EAR ASYMMETRIES IN A DICHOTIC TEST 1517 chords, as we were interested in extending the investigation of the relation between lateral eye movements and dichotic listening to a test not involving left hemisphere processing. More precisely, our hypothesis was that the left ear advantage usually found with dichotic chords is enhanced in LMs and reduced in RMs, and that this effect is not due to the facilitating influence of lateral eye movements occurring during the task. METHODS Stage 1, Selection of laterul mouers Subjects. One hundred and ten females, paid volunteers, participated in a fake study on “brain waves and cognition”, unaware that the actual focus of the study was on eye movements. All were right-handed without familial sinistrality as assessed by a handedness questionnaire [29]. Materials. Two parallel lists of questions were employed, each containing 24 verbal and 24 visuo-spatial questions, randomly alternated. The questions were drawn from a list used in a previous study on the effect of question content on direction of lateral eye movements [9]; examples are: “What is the meaning of the word affiliation?“, “What is the meaning of the proverb: strike while the iron is hot?“, “ In which direction would you fly to go from Japan to Vietnam?“, “Imagine a person facing the rising sun; with respect to him where is South?” Information crucial for reflection was withheld until the end of each sentence. Procedure. Each subject was seated in an experimental box (180 x 180 x 220 cm) with no asymmetrical stimuli on the horizontal axis, and had two electrodes on her forehead connected to a polygraph so as to simulate an EEG recording session. A female experimenter, sitting at a distance of 80 cm in front of the subject, asked the questions after getting into eye contact with her. During the entire session the eye movements were monitored by means of a video camera placed on a shelf high up and in front of the subject’s head (at a distance of 120 cm). The camera was set in such a way as to pass unnoticed as part of the normal laboratory equipment. The first lateral deviation of the gaze following the end of each question was considered as a reflective lateral eye movement. The scoring was carried out on the video-recordings by the same experimenter. Subjects were classified as right movers (RMs) or left movers (LMs) if they showed an idiosyncratic tendency to shift their gazes respectively to the right or left side irrespective of the verbal or spatial content of the questions. More specifically, the criteria used for selection were: (1) subjects had to show lateral shifts of the gaze in response to at least 50% of the questions; (2) at least 70% of these lateral shifts had to be in the same direction. Of the 36 subjects who satisfied these criteria, 33 came back for a retest session after a month and half. Out of these 33 subjects, 12 LMs and 11 RMs who showed RLEMs in the same direction in the retest session were recruited for the second stage of the study. The 10 remaining subjects did not reach the cut off criterion of 70% of lateral gaze shifts in the same direction and were not included in the second stage of the study; none of these subjects reached the cut-off criterion in the opposite direction (see Fig. 1). Stage 2. Dichotic experiment The mean age of the 23 subjects selected for the second stage of the study was the same in the two subgroups (LMs = 22.4; RMs = 22.4). None of them complained of any auditory impairment (no audiometric test was done), none was a professional or amateur musician. They received a small amount of money for participating in this second stage of the study. Materials. The dichotic chord test was a modified version of Gordon’s multiple choice test [15!, in which the original dichotic pairs had been rearranged in a single choice format with directed attention. This rearrangement was carried out in a previous study in order to reduce the memory and attentional load of the test and allow the detection of an ear advantage even in musically uneducated subjects [3&32]. The test consists of48 items separated by a 5 set inter-item interval. Each item is made up of the following sequence: one monaural chord (1.5 set), followed by a pause (1 set), followed by a dichotic pair of chords (1.5 set). Each chord consisted of the fundamental, third (minor or major), fifth and octave. The difference in pitch between the fundamentals of the dichotic chords never exceeded two semitones. In the case of matching of the monaural and the dichotic stimuli, the matching chord was always presented to the ear that had just received the monaural chord. Chords were generated and dichotically aligned by a Macintosh IIvx personal computer on the basis of a complex tone made-up of the first eight harmonics and yielding a flute-like sound without any vibrato or ornamentation. An example of one item is depicted in Fig. 2. In a study on 94 subjects 1301 the test had shown a significant left ear advantage of moderate size (r* =O.l 1) in both “naive” subjects and amateur musicians (non-professionals with at least 5 years of formal musical training). Females exhibited a smaller ear advantage than males (r’=O.O6); but the interaction between sex and ear of input wasnonsignificant (P=0.16).Thepercentageofsubjectsshowingleftearadvantagewas63.8% (+9.7”/0; C=95%). Subjects. P. SAN MARTINI ef a/ 1518 zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA lml- 8 Right movers 75. 00 0 0 0 SD25. 5 !z 0. 00 -25. 0 0 -500; -7s. Left Movers 00 &* -lBB- -100 -7s -58 -25 0 25 50 75 I00 Test Fig. 1. Scattergram of test and retest reflective lateral eye movement (RLEM) scores of the subjects selected as lateral movers in the first stage of the study. Scores for left movers are computed as: (number of RLEMs towards the left/total numbers of RLEMs) x (- 100). Scores for right movers are computed as: (number of RLEMs towards the right/total number of RLEMs) x 100. zyxwvutsrqponmlkjihgf PAUSE F m a j. F maj. G maj i@ Fig. 2. Diagrammatic description of the dichotic test: first a monaural chord is presented to either the left of the right ear; then a pair of different chords is presented simultaneously; the subject has to judge whether or not the monaural chord is contained in the dichotic pair. LATERAL EYE MOVEMENTS AND EAR ASYMMETRIES IN A DICHOTIC TEST zyxwvutsrqponmlkjihgfed 1519 Table 1. Summary of the analysis of variance Group x Ear on the number of recognitions and analysis of the simple effects Source of variation Group Ear Group x Ear d.f. F P 1, 21 1, 21 1, 21 1.oso 1.980 6.994 0.3171 0.1740 0.0152 Simple effects Group Group Ear at Ear at The test-retest r=0.703. reliability at left ear at right ear left movers right movers of the laterality 1, 21 1, 21 1,21 1,21 index, as assessed 2.707 0.147 8.581 0.734 after 1 month 0.115 0.008 on a sub-sample of 36 subjects. was Procedure. Subjects, wearing a pair of headphones, were comfortably seated at a table with their heads leaning on a chinrest; they were required to fixate a point on a screen in front of them and were asked not to shift their gaze during the test and to direct their attention to the ear which had just heard the monaural chord. They were informed that the ear receiving the monaural chord would change after every sixth trial. After eight practice items, subjects were presented with the dichotic test twice, the second time with the headphones rotated between the ears. The initial orientation of the headphones was counterbalanced across subjects. The tape was played to subjects on a Marantz P 1200 professional cassette recorder which allowed complete separation ofthe signals between the output channels. The level ofthe signal was calibrated to be identical at both earphones (70 dB as measured by a phonometer). Subjects had to judge whether the dichotic pair they had just heard contained the preceding monaural chord by saying “yes” or “no”. The dichotic test was administered by a different experimenter, blind to the group to which the subjects belonged. During the entire session the experimenter, sitting behind a screen and out of sight of the subject, monitored the eye movements of the subjects by means of the video camera and recorded direction and moment of any unwarranted gaze shift on a sheet of paper. RESULTS A 2 x 2 mixed design ANOVA [Group (LMs vs RMs) x Ear (R vs L)] was carried out on the number of correct recognitions. The analysis (see Table 1) yielded only a significant interaction Group x Ear. The analysis of the simple effects showed that this interaction was due to a left ear advantage in the left movers [F (1,21) = 8.58; P = O.OOS], while in the right movers there was no acoustic asymmetry (Fig. 3). The lack of a significant main effect of the ear was not unexpected, given the small number of subjects compared to the small expected size of the ear effect in females and given the moderating effect of the between group variable. Although subjects were instructed to fix a central point during each item of the dichotic test, they nevertheless made a few unwarranted eye movements during the task. In order to ascertain (a) whether during the dichotic task LMs had produced more leftward eye movements and RMs more rightward movements, and (b) whether these movements contributed to the differences in ear advantage between the two groups, the number of lateral eye movements of each subject was square root transformed and submitted to a 2 x 2 x 2 mixed design ANOVA [Group (LMs vs RMs) x Responses (Correct vs Incorrect) x Direction of eye movements (Right vs Left)]. A significant interaction Group x Direction of eye movements would suggest differences in the prevalent direction of unwarranted eye movements between the two groups. The interaction Group x Responses x Direction of eye movements could shed light on the second question. The interaction Group x Direction of eye movements [F(l, 21)=4.67; P-cO.051was significant, indicating that our subjects 1520 zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA P. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFE SAN MARTINI ef ul 36 35 34 33 32 ----.-- Left Ear u Right Ear 31 Left M overs Fig. 3. Mean number Right M overs of left and right ear recognitions in right and left movers. shifted their gaze in their usual direction even during the dichotic test. The interaction Group x Correctness x Direction of eye movements was not significant [F (1, 21) =0.26], indicating that unwarranted eye movements did not affect the ear advantage. Another datum goes against the hypothesis of a lateral facilitation as a consequence of lateral eye movements made during the test: the lack of correlation zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIH (r=0.077) between the number of correct acoustic recognitions and the number of eye movements towards the ear which the subject paid attention to. DISCUSSION Our results show that, during a dichotic task requiring processing of musical material, left movers exhibit a marked advantage of the left ear while right movers do not exhibit any consistent ear advantage. This finding is in agreement with the results obtained by Nielsen and Sorensen [27] on a dichotic digit recognition task and by Struthers, Charlton and Bakan [34] on a dichotic syllable recognition task, giving further support to the hypothesis that the tendency to consistently shift the gaze to one side is related to hemispheric asymmetries as measured by lateralized tests. The overall picture outlined by the present study and by both the above-mentioned studies is that the idiosyncratic direction of gaze affects dichotic laterality in the expected direction: as compared to left movers, right movers show a greater left ear advantage for verbal and numerical stimuli and a smaller right ear advantage for musical stimuli. It could be that the relationship between lateral gaze and hemispheric asymmetry found in this experiment may be extended to subjects showing less than 70% of lateral eye movements in one direction. To our knowledge only two studies have evaluated the relation between perceptual asymmetries in lateralized tests and laterality of gaze in unselected samples of right-handed subjects [lo, 281. The former correlated an index of laterality of gaze with performances in a tachistoscopic letter recognition task, the latter correlated lateral gaze with two dichotic (syllables and pitch contours) tests, neither of them finding significant correlations. Lack of a significant linear correlation between laterality of gaze and asymmetries in lateralized tests is not surprising as even dichotic listening and divided visual field tests show low intercorrelations (e.g. [7, 17, 20, 351). Our data show that lateral movers tend to shift their gaze in their usual direction also during a dichotic test and despite the instruction to fix a central point, i.e. in a condition that LATERAL zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA EYE M OVEM ENTS AND EAR ASYM M ETRIES IN A DICHOTIC TEST 1521 differs substantially from the condition in which their idiosyncratic lateral eye movements pattern was originally evaluated. In our experiment, however, such a tendency did not account, in any substantial amount, for the difference between right and left movers in auditory asymmetries, since there was no correlation between the number of correct acoustic recognitions and the number of congruent eye movements and there was no interaction Group x Correctness x Direction of eye movements. It may be argued that even though our subjects were looking straight ahead and were instructed to attend only to one ear, and even though their unwarranted eye movements did not affect dichotic performance, their tendency to watch to one side may still have yielded an asymmetrical covert allocation of attention toward the same side which may be responsible for their different perceptual asymmetries. This hypothesis, however, seems unlikely, since the same subjects participated in another study [S] in which they were given a test of covert orienting of attention and showed no significant difference in attentional costs and benefits between the right and the left visual hemifield. To date, the general pattern of results obtained testing lateral movers on valid lateralized tests seems to outline a coherent picture of the relationship between laterality of gaze and perceptual asymmetries, although the problem of its interpretation is far from being solved: do some people tend to look rightward or leftward because there is an imbalance in the level of hemispheric activation favouring one hemisphere or the other, or is it the other way round? Our data, being correlational in nature, cannot give an answer to this question of causation. Our findings are relevant to a question recently raised by Kim and Levine [20,21]. Having found in unselected subjects positive correlations between dichotic asymmetries for verbal, numerical and musical tasks, they concluded that performance in dichotic tests is influenced not only by the cognitive nature of the stimuli and by random error, but also by some stable individual trait, and pose the question of whether this trait is originated by central or peripheral processes. In the first case it could be attributed to differences in relative arousal levels of the left and right hemisphere [24]; in the second case it could be explained in terms of differences in pathways dominance (e.g. [ll, 231). 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