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Differences in visual attention and task interference between males and females reflect differences in brain laterality
Neuropsychologia 38 (2000) 508±519
www.elsevier.com/locate/neuropsychologia
Dierences in visual attention and task interference between males and females re¯ect dierences in brain laterality Heather Davidson a, Kyle R. Cave b,*, Daniela Sellner c a
Department of Psychology and Human Development, Vanderbilt University, Box 512-GPC, Nashville, TN 37203, USA b Department of Psychology, University of Southampton, High®eld, Southampton, SO17 1BJ, UK c Institut fuÈr Psychologie, 37073 UniversitaÈt CoÈttingen, Germany Received 16 February 1998; received in revised form 27 April 1999; accepted 4 May 1999
Abstract Two cognitive tasks (a letter memory task and a spatial memory task) designed to selectively activate the left or right hemisphere were combined with attentional probe tasks to measure how hemispheric activation aects attention to left and right hemi®elds. The probe task in Experiment 1 required the identi®cation of digits in the left and right hemi®eld. During the letter task, male subjects identi®ed more probes from the left hemi®eld than from the right. Their accuracy varied little across the two hemi®elds during the dots task. Experiment 2 tested whether this pattern is due to either spatial attention or interference in character processing. Instead of identifying digits, the probe task required subjects to respond to a black square that appeared in the periphery of the screen. For male subjects, the pattern was opposite of that from Experiment 1. During the letter task they responded faster to the probe in the right hemi®eld than in the left. Their response times were equivalent across the two hemi®elds during the dots task. These results indicate two separate eects of laterality in male subjects. The activation of one hemisphere produced more attention to the contralateral hemi®eld in Experiment 2, and the letter memory task interfered with the processing of other characters in the right visual ®eld more than those in the left visual ®eld in Experiment 1. Neither of these eects appeared in female subjects, corroborating earlier claims that female brains are less lateralized than male brains. # 2000 Elsevier Science Ltd. All rights reserved. Keywords: Visual selection; Character recognition; Hemispheres; Spatial probes; Sex dierences; Orienting
1. Introduction The early stages of visual processing in cortex are divided between the left and right hemispheres, with each hemisphere taking responsibility for the contralateral side of visual space. This study tests claims that functions of visual attention are also divided across the hemispheres, and also tests how attentional and other visual functions are in¯uenced by other brain processes occurring in the left and right hemispheres. * Corresponding author. Tel.: +44-2380-592234; fax: +44-2380594597. E-mail address: [email protected] (K.R. Cave).
Because previous studies have indicated dierences in brain laterality between male and female subjects, this study also tests for dierences in laterality between these two groups. 1.1. Evidence for hemispheric control of spatial attention Patients with visuo-spatial neglect are often described as having a de®cit in the ability to shift their attention towards the contralesional hemi®eld [32]. These de®cits suggest that each hemisphere may have a special role in controlling shifts of attention in the contralateral direction or to the contralateral side of space. Brain imaging studies show evidence of speci®c hemispheric activation during attention tasks in nor-
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H. Davidson et al. / Neuropsychologia 38 (2000) 508±519
mal subjects. An experiment by Corbetta et al. [10] indicated that the superior parietal and superior frontal cortex were more active when attention was shifted in a peripheral direction than when attention was ®xated on the center of the visual ®eld. They found a correlation between the shifting of attention in the peripheral direction and activation of regions in the superior parietal lobe around the postcentral sulcus. Moreover, the magnitude of the activation in the contralateral hemisphere was twice as large as the activation in the ipsilateral hemisphere. Another piece of evidence that each hemisphere specializes in contralateral shifts of attention came from a study with split-brain patients by Lavadas et al. [27]. The subjects' heads were tilted 908 to the right or left to disassociate left and right visual ®elds from the left and right sides of their environment. Under these conditions, the right hemisphere demonstrated an advantage for detecting stimuli on the left side of environmental space, and the left hemisphere showed an advantage for the right side of environmental space. Each hemisphere apparently plays a special role in attending to the opposite side of space, even when it does not correspond to the contralateral visual ®eld. Reuter-Lorenz and Kinsbourne [34] presented behavioral evidence that each hemisphere has a special role in allocating attention in the contralateral direction in normal subjects. They hypothesized that when one hemisphere is more active than the other, attention can be biased in the direction contralateral to the more activated hemisphere. They assumed that if a visual stimulus is presented in the right visual ®eld, then the activation in the left hemisphere should increase, and the tendency to allocate attention in the rightward direction should increase as well. To test this activation orienting hypothesis, they presented subjects with a line bisection stimulus presented tachistoscopically in only one hemi®eld on each trial. In this task, the subject bisects a horizontal line by drawing a small vertical mark intersecting the line at its midpoint. The deviation between the actual midpoint and the subject's mark re¯ects the attentional bias. With neglect subjects, the deviation between the subjective and real midpoint is usually quite high. Reuter-Lorenz and Kinsbourne, however, tested normal subjects and found small but signi®cant deviations. If the stimulus was presented in the right visual ®eld (presumably activating the left hemisphere), the midpoint was drawn too far to the right, re¯ecting a left side underestimation. In other words, the right portion of the line was better attended than the left. They found the opposite eect when a visual stimulus was presented in the left visual ®eld, activating the right hemisphere. These results suggest that visual stimuli may contribute to the activation of a hemisphere, therefore promoting an attention shift in the contralateral direction.
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Reuter-Lorenz and Kinsbourne's results are consistent with Kinsbourne's [23,24] earlier claims that both hemispheres work simultaneously to shift attention in opposite directions. He characterized neglect not as an attentional de®cit but as an attentional bias toward one side resulting from an imbalance in the system that controls lateral shifts of attention. Although Kinsbourne's ®ndings have not always been successfully replicated [2], his theoretical claims have been in¯uential in the study of hemispheric interactions. Kinsbourne [23] proposed that in normal subjects each hemisphere generates tendencies to shift attention in the contralateral direction. A visual stimulus can activate attention centers in both hemispheres, and the internal inhibitory con¯ict between them causes a balance between the tendencies for the hemispheres to shift attention in opposite directions. When the tendencies are balanced precisely, attention falls naturally in the center of the stimulus. Kinsbourne [24] attributed the fact that left neglect appears more often than right to a more powerful rightward than leftward tendency to shift attention in normal subjects. Kinsbourne [23] suggested that each hemisphere controls contralateral shifts because visual stimuli processed in the cortex can trigger excitation of the ipsilateral superior colliculus. Each colliculus inhibits the other, which causes a mutual inhibitory balance between hemispheres. Damage to one hemisphere, such as in neglect, interferes with the excitatory inputs to the colliculus, disrupting the balance with the colliculus on the opposite side. Since the damaged hemisphere is inhibited, the undamaged hemisphere has less inhibition and produces a bias to shift attention in the contralateral direction. Therefore, the contralesional side of the visual ®eld is neglected. Reuter-Lorenz and Kinsbourne's results were just as predicted by the activation orienting hypothesis, but they might also be explained by more speci®c attentional interactions. Each stimulus was presented in only a single hemi®eld, in order to activate the contralateral hemisphere. When the stimulus appears alone in the left hemi®eld, for example, it will probably induce an attention shift to the left of the visual ®eld. This global attention shift might bias the subject to attend to the left side of the stimulus. In other words, the allocation of attention in a global context might bias attentional allocation in a local context, independently of the degree of neural activation within the left hemisphere. The experiments presented below tested whether other tasks that are performed primarily within one hemisphere or the other would bias spatial attention to visual stimuli that are equally balanced across both hemi®elds. Two tasks were chosen that have been shown by PET studies to activate the left or right hemisphere [19,36,37]. The left hemisphere was activated with a letter memory task, and the right
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hemisphere was activated with a spatial memory task. Neither task explicitly drew attention to either side of the visual ®eld. 1.2. Evidence for gender dierences in brain laterality There is evidence from a number of dierent sources that interactions between hemispheres vary between male and female subjects (see Hellige [13], Iaccino [18], and Springer and Deutsch [38] for reviews). Females tend to perform better on linguistic tests, including articulation speed, verbal ¯uency, grammar, and verbal production, while males tend to score higher on spatial tests, including mathematics, maze performance, and mental rotation [12]. Levy [28±30] suggested that females represent language in both hemispheres, which improves communication abilities but impairs spatial skills. Bryden [7] concluded that the left hemisphere is dominant for speech and that the right hemisphere is dominant for spatial tasks more often in right-handed males than in right-handed females. A variety of perceptual experiments have compared detection in the left and right visual ®elds by male and female subjects under dierent ®xation conditions. Although some studies ®nd no asymmetries in males, Iaccino [18] reviews many that have indicated an LVF advantage in males for nonverbal materials such as photographed faces, and RVF advantages for verbal materials, indicating a stronger lateralization of higher perceptual functions in males than in females. Dichotic listening studies have also indicated stronger lateralization of verbal processing in males [25], although in general the results from auditory lateralization experiments have been mixed and sometimes confusing. Hellige [13] summarizes reviews by Hiscock et al. [17] and Hiscock et al. [15,16] of 37 auditory, visual, and tactile tests. Twenty-®ve of the studies reviewed indicated greater laterality in males than females, which, as Hellige observes, is a statistically signi®cant proportion. Laterality dierences have also been found between males and females in measures of brain activity, although these ®ndings have also been mixed and sometime confusing. In one of the more recent studies, Shaywitz et al. [35] examined the brain activity in right-handed males and females during phonological tasks with functional MRI. They found that in males, brain activation was lateralized to the left inferior frontal gyrus. In females the pattern of activation was 1 Lauber et al. subsequently tested additional subjects in these tasks, but they were unable to replicate these dierences between male and female subjects (Lauber, personal communication). Whether or not these two types of tasks reliably produce dierent brain activations in males and females, the fact that they dierentially activate left and right hemispheres has been demonstrated in multiple experiments [19,36,37].
very dierent, engaging more diuse neural systems that involve both the left and the right inferior frontal gyrus. Dierences in brain lateralization between males and females was also found in a PET study by Lauber et al. [26] that included two tasks very similar to those used in the experiments presented below. In Lauber et al.'s study, a letter-memory task increased the activation in certain areas of the left hemisphere in male subjects. Each subject was shown a series of letters on a computer, presented one at a time. After each presentation the subject was asked if the current letter on the screen was the same letter as the letter three trials back. The case of the letters was varied to force matching by letter identity rather than shape. Male subjects showed a signi®cantly higher level of activation in the left hemisphere and no signi®cant right hemisphere activation in the frontal lobes. Both hemispheres were active in the female subjects. The stimulus in Lauber et al.'s spatial memory task consisted of a pattern of three dots in random locations around a ®xation cross. After the dots disappeared, the subject was presented a probe circle and asked to respond YES or NO, by pushing a button, indicating whether a dot had appeared in the circle's location. The male subjects had higher activation levels in the right hemisphere than in the left. The highest region of activity for males was right area six, followed by the right posterior parietal regions. The female subjects showed bilateral activation across both hemispheres during the spatial working memory task. In general, Lauber et al.'s ®ndings from the verbal and spatial tasks suggest that male subjects are more lateralized than female subjects for both tasks1. The asymmetries in brain activation demonstrated by Lauber et al. suggest that we can use these two working memory tasks to activate each hemisphere individually. However, the dierent patterns of activation between male and female subjects require that we examine the data from both groups separately. If Lauber et al.'s ®ndings do re¯ect a real dierence in cortical organization between males and females, then we can expect to ®nd lateralized attentional eects with these tasks only in the male subjects. In our experiments, each subject performed modi®ed versions of these letter memory and spatial memory tasks, each in a separate block of trials. Only data from right-handed subjects are presented here. On each trial the memory task was combined with a spatial probe task to measure the allocation of spatial attention while the letters or the dot locations were retained in working memory. In Experiment 1 the spatial probes were similar to the letter array used by Kim and Cave [20,22] and by Bichot et al. [1]. In Kim and Cave's ®rst experiment [20], a search array (an array of squares and circles) was presented brie¯y
H. Davidson et al. / Neuropsychologia 38 (2000) 508±519
around a ®xation cross. The subject was then asked to press a button to indicate whether the target had appeared. Then a circular array of black letters was presented brie¯y. Using the mouse, subjects reported the letters they had seen in the display. Kim and Cave [22] and Bichot et al. used a similar procedure. In all of these studies, letters were more often correctly identi®ed when they were in the location previously occupied by a search target. In each trial of Experiment 1, subjects ®rst saw the primary (memory) task stimulus, either a letter or an array of dots, in the center of the display. Soon after it appeared, four digits appeared brie¯y in the periphery, two in the left hemi®eld and two in the right. Subjects reported all four digits, and then gave their response for the memory task. Based on Kim and Cave's results, we expect that dierences in the accuracy in reporting the probe digits will re¯ect dierences in spatial attention. We can test for lateralized attentional eects by comparing accuracy for left and right hemi®eld digit reports. 2. Experiment 1 2.1. Methods 2.1.1. Subjects Fifty-two male and ®fty-one female undergraduates from Vanderbilt University participated in this experiment. Only right-handed subjects were used. Each subject had normal or corrected to normal vision.
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The probe stimuli in both right and left hemisphere tasks consisted of four black digits, numbers 0 to 9, appearing for 30 ms. Each digit was in 22 point bold Monaco font. The four digits were each 7 mm tall and were placed in a square formation 87 mm on each side, so that each digit was 62 mm from ®xation. 2.1.4. Procedure The two dierent primary tasks were separated into two separate blocks of trials. Half of the subjects began with the left hemisphere (letters) task and the other with the right hemisphere (dots) task. In each block the subject viewed a series of displays. In each trial of the dots task, the subjects were instructed to keep their eyes ®xed on the ®xation cross throughout each trial (see the right side of Fig. 1). Two small red dots appeared on the middle of the screen for 180 ms. The locations of these red dots were dierent for each trial. As part of the primary task, the subject was asked to remember the locations of the dots on the screen. After the two dots disappeared, four digits appeared. The SOA (the delay between the onset of the primary stimulus, the dots, and the onset of the probe stimulus, the digits) was either 195, 240, or 285 ms. The digits were located farther in the periphery than the dots. As the subject continued to remember the position of the dots, he or she reported the digits using the mouse to mark the chosen digits on a list on
2.1.2. Apparatus Three Macintosh IIsi computers were used, each with a 13 inch Applecolor monitor and attached mouse. Subjects used a chin rest to keep them approximately 50 cm from the computer screen. 2.1.3. Stimuli A ®xation stimulus was present in the center of the display. For the dots task it was a cross, 4 mm wide and tall, and for the letters task it was a black box 13 mm wide and 18 mm high. The primary stimuli in the dots (right hemisphere) task consisted of two solid red dots with a diameter of 3 mm. The red dots appeared in dierent locations around a ®xation cross. There was at least 11 mm between every pair of dots and between each dot and the ®xation cross. The maximum distance between each dot and the ®xation cross was 28 mm. A green ring, 6 mm in diameter, appeared for the length of time it took the subject to respond to the primary task. The primary stimuli in the left hemisphere task consisted of an 11 mm red letter in 38 point bold Monaco font, either lower or upper case, that appeared in the box.
Fig. 1. These diagrams symbolize the sequence of displays for the two memory tasks in Experiment 1. See the text for the stimulus dimensions.
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the screen. Each subject was required to report all four digits on each trial, guessing if necessary. After the subject reported the digits, a small green circle appeared on the screen. The subject used the mouse to click a YES or NO box indicating if one of the red dots had been located within the position of the green circle. Following this presentation, a display appeared for 2 s, indicating which digits were reported correctly. The letters task was very similar to the dots task. Before the trials began, two letters were shown to the subject, one after another, to start the sequence of letters to be remembered. During each trial the subject was asked to ®xate on a black box (see the left side of Fig. 1). An upper or lower case letter appeared in the box for 180 ms. The subject's primary task was to decide whether that letter was the same letter as the letter that appeared two trials back, ignoring the case of the letter. Soon after the letter disappeared, four probe digits appeared, just as in the dots task. The SOA's between primary and probe stimuli for the letters task were the same three values used in the dots task. As the subjects retained the most recent letters in their memory, they were asked to identify the four digits, using the mouse. After reporting the digits and observing those which they answered correctly, the subject was asked to select with the mouse a YES or NO button indicating whether the letter presented on this trial matched the letter appearing two trials back. In both blocks of trials of this experiment the subjects were encouraged to take as much time as necessary to respond. Each block began with 15 trials of practice (more if the subject or experimenter thought it was necessary). Each block consisted of 72 trials (not including practice). The subjects were oered a break near the middle of each block.
analyses. In the letters task, one male subject and two female subjects produced more than 35% errors and in the dots task ®ve male subjects and twelve female subjects produced more than 35% errors. A total of ®ve male subjects and fourteen female subjects were discarded from the analysis. The data for males and females were analyzed separately. 2.2.2. Probe task The percentages of incorrect probe digit responses at each location were calculated separately for male and female subjects. These data were then analyzed to test whether the frequency with which subjects reported digits from the two sides of visual space varied between the two primary tasks. The probe accuracy data were submitted to fourway ANOVAs with dots or letters task, left or right hemi®eld, SOA, and upper and lower hemi®eld as factors. The analysis for the male subjects revealed a signi®cant interaction between hemi®eld and task (see Fig. 2), but the direction of the eect was opposite to what was expected. Males correctly reported fewer letters from the right hemi®eld than from the left during the letters task, and slightly fewer from the left hemi®eld than from the right during the dots task, F(1,44)=6.008, p < 0.05. Assuming that the two tasks activated the left and right hemispheres in the male subjects as in previous PET studies, then activating a hemisphere in this task produced better performance in the ipsilateral hemi®eld rather than the contralateral. The female subjects showed no hint of the interaction between memory task and probe hemi®eld that appeared in the male data, F < 1. In both tasks, the females reported slightly more digits in the right hemi®eld than the left (see Fig. 3). Unlike the males, the
2.1.5. Design The dependent variable in this experiment was the accuracy (percent error) for reporting digits at each location. Data from male and female subjects were analyzed separately. Each analysis included four factors: the primary task (dots or letters), probe digit hemi®eld (left of right), probe digit location within the hemi®eld (upper or lower), and SOA. 2.2. Results 2.2.1. Primary (memory) task The mean accuracy in the letters (left hemisphere) task was 86% for male subjects and 83% for female subjects. In the dots (right hemisphere) task, the mean accuracy for male subjects was 74% and for female subjects 71%. If any subject made more than 35% errors in either primary task, that subject's data were discarded from both right and left hemisphere task
Fig. 2. Error rates for identifying probe digits from the male subjects in Experiment 1.
H. Davidson et al. / Neuropsychologia 38 (2000) 508±519
Fig. 3. Error rates for identifying probe digits from the female subjects in Experiment 1.
females showed no evidence that these tasks produced dierences in visual processing across hemi®elds by activating one hemisphere more than the other. 2.2.3. Other signi®cant eects Both the male and female analyses showed several additional main eects and interactions. Male subjects made more mistakes in reporting probes during the letters task than the dots task, F(1,44)=15.1, p < 0.001, as did female subjects, F(1,36)=26.1, p < 0.001. Perhaps the letters task is generally more demanding than the dots task. However, the error rate of reporting the letters was lower than the error rate of reporting the dots. During both tasks, male subjects made more errors in reporting digits from the right hemi®eld than from the left, F(1,44)=4.4, p < 0.05. There was no main eect of hemi®eld in the female subjects; however, they reported slightly fewer digits correctly from the left hemi®eld than the right, F < 1. Fewer digits were reported from the lower hemi®eld than the upper, both for males, F(1,44)=23.4, p < 0.001, and females, F(1,36)=14.5, p < 0.001. This result may re¯ect an attentional bias to the upper hemi®eld. Some researchers have found that normal subjects will bisect a vertical line slightly above the midpoint [33], possibly indicating such a bias. For both male and female subjects, the dierence in performance between upper and lower ®eld probes was greater with the letters task than with the dots task; males: F(1,44)=4.4, p < 0.05; females: F(1,35)=10.8, p < 0.01. Probe error rates varied signi®cantly with SOA for both males, F(2,88)=7.3, p < 0.01, and females, F(2,72)=5.4, p < 0.01. For females, errors decreased as the time between the primary stimulus and the probes increased. For males, errors were highest for
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the shortest SOA and lowest for the intermediate SOA. For both males and females, however, varying the SOA only produced an overall dierence in error rate of 2 or 3%. For the female subjects there was a signi®cant interaction between SOA and probe hemi®eld, F(2,72)=3.3, p < 0.05. For the shortest and longest SOA's, responses were most accurate for probes on the right, but for the intermediate SOA they were slightly more accurate for those on the left. For each SOA, however, the dierence between the two hemi®elds was only 1 or 2%. There was no hint of such an interaction in the male data, F < 1. The male analysis also showed a four-way interaction between task, SOA, hemi®eld, and upper versus lower visual ®eld, F(2,88)=5.9, p < 0.01. For all three SOAs, the letters task produced more errors than the dots task, and these extra errors occurred mainly for digits on the right side rather than those on the left. However, the distribution of these extra errors across upper and lower visual ®elds diered with the SOA. In the shortest and longest SOAs (195 and 285 ms), the letters task produced many more errors for digits in the lower right quadrant, while for the middle SOA (240 ms) the extra errors associated with the letters task were distributed across the lower right, upper right, and lower left quadrants. No such interaction appeared in the females analysis, F < 1. Assuming that this interaction re¯ects a real dierence across SOAs, it does not appear to detract from attentional dierences between hemi®elds and the dierences between male and female subjects described earlier. 2.2.4. Comparing results across male and female subjects The data from both male and female subjects were combined in a single ANOVA to test whether the interaction of task and hemi®eld diered signi®cantly between the two subject groups. Although the dierences between the male and female data in Figs. 2 and 3 are rather striking, the three-way interaction between task, left versus right hemi®eld, and sex did not reach signi®cance, F(1,80)=2.1, p > 0.1. Although the interaction between these three factors was not signi®cant, these factors were part of a signi®cant ®ve-way interaction between task, SOA, left versus right hemi®eld, upper versus lower hemi®eld, and sex, F(2,160)=3.4, p < 0.05. From this, we concluded that the three-way interaction might vary according to the time between the primary stimulus and the digit probes. Therefore, each SOA was analyzed separately. The third SOA, 285 ms, did show a signi®cant three-way interaction between task, hemi®eld, and sex, F(1,80)=5.4, p = 0.023. For the ®rst two SOAs, 195 and 240 ms, the three-way interaction between dots or letters task, left versus right hemi®eld, and sex was not
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Table 1 Percentage of digit probes reported correctly in Experiment 1
Female verbal Female spatial Male verbal Male spatial
195 ms SOA Left probes
Right probes
240 ms SOA Left probes
Right probes
285 ms SOA Left probes
Right probes
34 30 32 31
33 26 37 29
32 28 31 28
33 28 33 29
33 26 30 28
29 25 36 28
signi®cant, although the trend was in the same direction. The probe data are presented separately for these three SOAs in Table 1. Apparently the nature of the primary task does aect males and females dierently, but the dierences appear most strongly after subjects have had time to become engaged in the primary task. This analysis produced no other signi®cant interactions including sex as a factor. 2.3. Discussion The two primary tasks aected the processing of left and right ®eld stimuli dierently in male subjects, but not in females, as expected. However, we expected lower accuracy for digits reported in the hemi®eld ipsilateral to the activated hemisphere in males, but instead accuracy was lower for the contralateral hemi®eld. This pattern seems quite stable, because we found similar trends in two other slightly dierent versions of the experiments2. There are three possible explanations for these dierences: the tasks employed to activate the hemispheres may have been interfering with attentional mechanisms rather than activating them, the tasks may have been interfering with mechanisms in each hemisphere that process characters, or subjects may be more likely to miss digits in the right hemi®eld when the error rate is high. According to the ®rst explanation, the primary tasks were successful in activating particular mech2 The two previous experiments varied from the present study in certain details of the tasks. In the ®rst experiment the displays for the spatial memory task consisted of three dots rather than two, which resulted in very low accuracy rates for the spatial memory task. With such a dicult dots task, subjects may not have been able to perform the probe task well enough to give good measures of spatial attention. In the second experiment, subjects were instructed to report two probe digits on each trial rather than four. In this case, subjects performed the probe task too well. Accuracy was so high that the probe data yielded less information about the allocation of attention. Despite the problems with these earlier experiments, the results from each were similar to those of the ®nal experiment. In both earlier experiments, males showed similar trends toward an interaction between memory task and probe hemi®eld, although it did not achieve signi®cance in either. The female data for one experiment showed a weaker trend in the same direction, and in the other showed a weak trend in the opposite direction.
anisms in the target hemispheres, and they pulled resources away from the attentional mechanisms in the same hemisphere. For example, during the letters task in male subjects, the letter stimuli activated the left hemisphere's areas for identifying and remembering sequences of characters, and this activation drew resources away from the attention mechanism in the left hemisphere. If Kinsbourne's [23] theory of hemispheric balance is correct, lack of activation in the left hemisphere would disrupt the balance, causing the attentional mechanisms in the right hemisphere to dominate and shifting attention contralaterally. Therefore, more digits would be attended in the left hemispace than in the right during a letter task. The second possible explanation does not involve spatial attention, but interference between two tasks relying on the same left-hemisphere resources [6,11,31,39,40]. Both hemispheres may have mechanisms for identifying and remembering characters, but the left hemisphere's mechanisms may be more developed because of its specialization for language. The idea of a single mechanism for recognizing both letters and digits is consistent with conclusions from Boles [3±5] based on factor analyses of the dierences in lateralization across subjects in a wide range of cognitive tasks. Based on his ®ndings, Boles composed a list of general cognitive functions, and claimed that each general function would vary in lateralization from subject to subject independently of other functions. Interestingly, Boles proposed a single cognitive mechanism for all visual lexical tasks, including both those involving letter stimuli and those involving digit recognition. Boles suggests that visual lexical processing is more strongly associated with the left hemisphere, so it is no surprise that our letters task might be performed primarily in the left hemisphere, limiting that hemisphere's ability to identify digits appearing in the right hemi®eld. Our dots task seems to ®t best with Boles' spatial positional function, which is independent of the visual lexical function and is typically associated with the right hemisphere. This hypothesis may explain why both male and female subjects reported more digits overall during the dots task than during the letters task, because brain mechanisms used to remember the
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dots will be less likely to interfere with those involved with processing the digits. A ®nal explanation arises from the observation that the letters task interfered more with digit reports than the dots task. When subjects are limited in the number of digits they can report, they may be more likely to report those on the left because of habits developed in reading. This explanation predicts a similar left hemi®eld advantage if the dots task is made more dicult. In a previous experiment described in footnote 2, we did use a more dicult dots task. In this experiment, the probe error rate with the dots task was similar to that in the letters task, but in the male subjects there was still no left hemi®eld advantage with the dots as there was with the letters. Thus, the results from the preliminary experiment argue against this alternative explanation. Furthermore, it is dicult to see why this `start from the left' strategy would be limited to males. 3. Experiment 2 Experiment 2 was designed to distinguish between the two possible explanations for Experiment 1. The digit probes were replaced with a single dot probe, as used by Kim and Cave [20], Cave and Zimmerman [8], Cepeda et al. [9] and Kim and Cave [21]. Soon after the primary stimulus, a small square probe stimulus appeared at a single location on half the trials. When subjects detected the probe, they pressed a button as quickly as possible. Dierences in response time to dot probes at dierent locations re¯ect dierences in spatial attention. The dot probe provides a second attentional measure, and unlike the digit probes, it will not be susceptible to interference in character recognition. If the ®rst (attentional) explanation for Experiment 1's results is correct, then the probe RT's in Experiment 2 should show a similar advantage for locations ipsilateral to the activation from the primary task.
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3.1.2. Apparatus As in Experiment 1, three Macintosh IIsi computers, each with a 13 inch Applecolor monitor and attached mouse were used. Subjects used a chin rest to keep them approximately 58 cm from the computer screen. A response box connected to the computer had two buttons on the left labeled YES and NO, and one button on the right labeled BLACK SQUARE. 3.1.3. Stimuli The primary stimuli were identical to those in Experiment 1. The probe was a black square 3 mm on each side. When it appeared, it was 87 mm from ®xation at one of the four corners of an imaginary square around ®xation. 3.1.4. Procedure The primary tasks were identical to those in Experiment 1. Each primary stimulus was visible for 75 ms. Half of the subjects started with the letter task ®rst, the other half with the dots task. Instead of digit identi®cation, the subjects were required to respond as quickly as possible to the black square that ¯ashed in the periphery of the screen on half of the trials. The SOA [the delay between the onset of the primary stimulus (the letter or dots) and the onset of the probe stimulus (the black square)] was either 90, 135, or 180 ms, and the probe was visible for 30 ms. The subjects were asked to press a button on the response box as soon as the black square appeared (see Fig. 4). The same button was pressed regardless of the probe's lo-
3.1. Methods The attentional probe task in Experiment 2 did not require character processing. The probe was a black square, and the dependent variable was the response time for detecting the black square. This new probe task allowed the measurement of spatial attention while avoiding the possibility of interference in identifying and remembering characters. 3.1.1. Subjects Forty-four female and twenty-nine male undergraduates of the Vanderbilt University participated in the experiment. All were right-handed and each subject had normal or corrected to normal vision.
Fig. 4. These diagrams symbolize the sequence of displays for the two memory tasks in Experiment 2. See the text for the stimulus dimensions.
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cation. Each trial block began with at least 15 trials of practice. Each block consisted of 192 trials. The subjects were oered two breaks during the experiment. 3.1.5. Design The dependent variable in this experiment was the response time to the probe. Data from male and female subjects were analyzed separately. Each analysis included the same four factors as the analyses in Experiment 1.
3.2. Results The analysis for Experiment 2 was similar to that for Experiment 1. 3.2.1. Primary task The mean accuracy in the letters (left hemisphere) task was 92% for male subjects and 91% for female subjects. In the dots (right hemisphere) task, the mean accuracy for male subjects was 95% and for female subjects was 92%. Data from subjects who scored less than 65% correct in either primary task were discarded from both right and left hemisphere probe analyses. A total of three male subjects and ®ve female subjects were discarded from the analysis. 3.2.2. Probe task Every subject was at least 65% accurate on the probe task. The male analysis revealed a signi®cant interaction between left versus right hemi®eld and primary task F(1,28)=10.0, p < 0.01, and this time it was in the direction predicted by the activation orientation hypothesis. Males subjects responded faster to the probes in the right hemi®eld than to the left hemi®eld
Fig. 5. Response times for detecting probes from the male subjects in Experiment 2.
during the letters task (see Fig. 5), while left and right response times were almost equal for the dots task. The female subjects showed no hint of this type of interaction between primary task and left versus right hemi®eld, F(1,43)=1.4, p < 0.2. In both tasks, the females responded faster to the probe appearing in the right hemi®eld than the left (see Fig. 6). In fact, what trend there is in the female data is in the opposite direction from the male interaction. 3.2.3. Other signi®cant eects Both male and female subjects were generally faster in their probe responses during the dots task than during the letters task; F(1,43)=16.1, p < 0.001 for females and F(1,28)=30.0, p < 0.001 for males. As in Experiment 1, the spatial memory task seems to be less demanding than the verbal memory task. Responses were generally faster for probes on the right than on the left; F(1,43)=32.7 p < 0.001 for females and F(1,28)=15.2, p < 0.001 for males. Male subjects were faster for probes in the upper visual ®eld than in the lower visual ®eld, but only during the letters task and not during the dots task, F(1,28)=12.2, p < 0.01. Female subjects showed no signi®cant dierences between upper and lower visual ®elds. Probe response times varied across the three dierent SOAs in females F(2,86)=8.2, p < 0.001, but not in male subjects. The response time for females was longer for the fastest probes (90 ms SOA) than for probes that appeared later. 3.2.4. Comparing results across male and female subjects As in Experiment 1, another analysis combined the data of male and female subjects together. The threeway interaction between task, hemi®eld and sex was
Fig. 6. Response times for detecting probes from the female subjects in Experiment 2.
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signi®cant, F(1,71)=10.6, p < 0.01, emphasizing the dierence between males and females in the way that attention is aected by the two primary tasks. Other eects were consistent with what was seen in the male and female analyses. The way in which the two primary tasks aected probes in the upper and lower visual ®elds diered signi®cantly between males and females, F(1,71)=11.4, p < 0.01. There were no other signi®cant eects involving subject gender. 3.2.5. Probe errors The mean probe error rate was below 5% for both male and female subjects. Analyses of the probe response errors revealed no hint of a speed accuracy trade-o that would raise doubts about the conclusions from the response time data. The male subjects produced no signi®cant main eects or interactions. Female subjects made more errors during the verbal task in the lower visual ®eld and more errors during the spatial task in the upper visual ®eld, F(1,43)=5.5, p < 0.05. 3.3. Discussion The second experiment was designed to determine if the results of Experiment 1 were due to character processing interference or attentional interference. The results revealed an interaction of task and hemi®eld that was opposite to that in Experiment 1. The task that was designed to activate the left hemisphere in males increased attention to the contralateral hemi®eld. The pattern in Experiment 2 suggests that the activation of areas within one hemisphere can facilitate attention to the contralateral hemi®eld as originally predicted, and thus the results from Experiment 1 can be attributed to interference of character processing rather than attentional interference. This account of the dierence between the probe tasks seems plausible in light of Bole's [5] results when he used a task somewhat similar to our dots probe task. Boles reported only weak evidence of lateralization of this task in the left hemisphere, and no evidence that it correlated with the visual lexical or spatial positional functions. Therefore, Boles' prediction would probably be consistent with our results showing that the dots probe task does not interfere much with either the letters or dots task. The pattern of response times in Fig. 5 seems to show that the letter (left hemisphere) task produces an attentional advantage for the right hemi®eld over the left, while the dots (right hemisphere) task has no eect on attention. However, there may be a main eect that speeds responses to all probes on the right side relative to those on the left, which could cancel out the attentional eect of the dots task. Thus, while we cannot be certain of the details of the interactions between these tasks and spatial attention, we can be
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con®dent that these two tasks aect attention to the left and right hemi®elds in very dierent ways. 4. General discussion The two tasks in these experiments demonstrate both facilitation and interference between dierent processes within a hemisphere. Experiment 1 showed that in male subjects the identi®cation and memory of letters for the verbal task interfered with the identi®cation and memory of digits in the left hemisphere, as illustrated in Fig. 7. The results of Experiment 2 revealed that the activation of left hemisphere areas in male subjects during the verbal task facilitated the attention mechanism in that hemisphere, as illustrated in Fig. 8. Attention was shifted to the contralateral hemi®eld and caused a shorter probe response time in that hemi®eld. Previous studies have shown both hemispheric facilitation and interference as well. For example, Hellige and Cox [14] found that remembering a short list of nouns could facilitate visual recognition of right hemi®eld stimuli, while remembering a longer list interfered with right hemi®eld recognition. These two eects provide new insights to two dierent aspects of visual perception and its implementation in the brain. The facilitation in Experiment 2 serves as new evidence for the idea that attentional mechanisms in the two hemispheres compete to pull attention in opposite directions. It also shows that the allocation of attention to one set of stimuli is aected by other brain processes that are triggered by unrelated tasks with unrelated stimuli. The pattern of interference in Experiment 1 suggests that in male subjects a task that
Fig. 7. Hemispheric interactions during Experiment 1.
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Acknowledgements Thanks to Narcisse Bichot, William Caul, Carolyn Backer Cave, Min-Shik Kim, Erick Lauber, Patricia Reuter-Lorenz, Je Schall, Amy Shelton, Ed Smith, and Ken Sobel for comments. Thanks also to Paul Russell and Tom Birkett for providing software to control the Macintosh response keys and a design for the response key interface, and to Lonny Shimp for building the response keys. This work was supported in part by Grant P30-EY08126 from NEI awarded to the Vanderbilt Vision Research Center. References
Fig. 8. Hemispheric interactions during Experiment 2.
requires identifying and remembering letters will be assigned to the left hemisphere, where it will interfere with processing of other characters in the right visual ®eld more than those in the left. Although the eects in the two experiments were in opposite directions, they were similar in that female subjects showed no hint of interaction between task and hemi®eld in either experiment. Together these experiments provide two new pieces of evidence that there are basic dierences between male and female subjects in the performance of perceptual and cognitive tasks. The similarity in performance across hemi®elds in females may occur because female brains, or at least the mechanisms responsible for these tasks, are less lateralized than male brains. Therefore, the tasks did not exclusively activate one hemisphere in the female subjects, but rather activated both hemispheres, and the attentional mechanisms in both hemispheres were activated more or less equally. These results have implications for at least three dierent areas of research. First, they demonstrate new aspects of the division of attentional control across hemispheres. They demonstrate that control of attention is at least somewhat in¯uenced by other unrelated brain events, and that these in¯uences can result in attentional dierences between men and women. Second, they provide new evidence on how the work of processing symbolic characters is distributed across the cortex. Third, they illustrate two new perceptual tasks for studying laterality dierences between males and females. These dierences have been elusive and dicult to pin down in the past, and these new experimental methods should help to determine what dierences there are in brain organization and how these dierences aect perceptual and cognitive processing.
[1] Bichot NP, Cave KR, Pashler H, Visual selection mediated by location: feature-based selection of noncontiguous locations, Perception and Psychophysics 1999;61:403±23. [2] Boles DB. Laterally biased attention with concurrent verbal load: multiple failures to replicate. Neuropsychologia 1979;17:353±61. [3] Boles DB. Factor analysis and the cerebral hemispheres: pilot study and parietal functions. Neuropsychologia 1991;29:59±91. [4] Boles DB. Factor analysis and the cerebral hemispheres: temporal, occipital and frontal functions. Neuropsychologia 1992;30:963±88. [5] Boles DB. Factor analysis and the cerebral hemispheres: ``unlocalized'' functions. Neuropsychologia 1996;34:723±36. [6] Boles DB, Law MG. A simultaneous task comparison of dierentiated and undierentiated hemispheric resource theories. Journal of Experimental Psychology 1998;24:205±15. [7] Bryden MP. Laterality: Functional Asymmetry in the Intact Brain. New York: Academic Press, 1982. [8] Cave KR, Zimmerman J. How spatial attention is allocated in letter search before and after practice. Psychological Science 1997;8:399±403. [9] Cepeda NJ, Cave KR, Bichot NP, Kim M. Spatial selection via feature-driven inhibition of distractor locations. Perception and Psychophysics 1998;60:727±46. [10] Corbetta M, Miezin FM, Shulman GL, Petersen SE. A PET study of visuospatial attention. The Journal of Neuroscience 1993;13:1202±26. [11] Friedman A, Polson MC, Dafoe CG, Gaskill SJ. Dividing attention within and between hemispheres: testing a multiple resources approach to limited-capacity information processing. Journal of Experimental Psychology: Human Perception and Performance 1982;8:625±50. [12] Halpern D. Sex Dierences in Cognitive Abilities. Hillsdale, NJ: Erlbaum, 1986. [13] Hellige JB. Hemispheric Asymmetry: What's Right, What's Left. Cambridge, MA: Harvard University Press, 1993. [14] Hellige JB, Cox PJ. Eects of concurrent verbal memory on recognition of stimuli from the left and right visual ®elds. Journal of Experimental Psychology: Human Perception and Performance 1976;2:210±21. [15] Hiscock M, Hiscock CK, Inch R. Is there a sex dierence in visual laterality? Paper presented at the Annual Meeting of the International Neuropsychological Society, San Antonio, TX, 1991. [16] Hiscock M, Hiscock CK, Inch R. Is there a sex dierence in visual laterality? Paper presented at the Annual Meeting of the International Neuropsychological Society, San Diego, CA, 1992.
H. Davidson et al. / Neuropsychologia 38 (2000) 508±519 [17] Hiscock M, Hiscock CK, Kalil KM. Is there a sex dierence in auditory laterality? Paper presented at the Annual Meeting of the International Neuropsychological Society, Kissimmee, FL, 1990. [18] Iaccino JF. Left Brain±Right Brain Dierences: Inquiries, Evidences, and New Approaches. Hillsdale, NJ: Erlbaum, 1993. [19] Jonides J, Reuter-Lorenz PA, Smith EE, Awh E, Barnes LL, Drain M, Glass J, Lauber EJ, Patalano AL, Schumacher EH. Verbal and spatial working memory in humans. The Psychology of Learning and Motivation 1996;35:43±88. [20] Kim M, Cave KR. Spatial attention in visual search for features and feature conjunctions. Psychological Science 1995;6:376±80. [21] Kim M, Cave KR, Top-down and bottom-up attentional control: on the nature of interference from a salient distractor, Perception and Psychophysics 1999;61:1009±23. [22] Kim M, Cave KR, Grouping eects on spatial attention in visual search, Journal of General Psychology, 1999 (in press). [23] Kinsbourne M. Lateral interactions in the brain. In: Kinsbourne M, Smith WL, editors. Hemispheric Disconnection and Cerebral Function. Spring®eld, IL: C. C. Thomas, 1974. p. 239±59. [24] Kinsbourne M. Mechanisms of unilateral neglect. In: Jeannerod M, editor. Neurophysiological and Neuropsychological Aspects of Spatial Neglect. New York: North Holland, 1987. p. 69±86. [25] Lake A, Bryden MP. Handedness and sex dierences in hemispheric asymmetry. Brain and Language 1976;3:266±82. [26] Lauber E, Jonides J, Koeppe RA, Awh E, Schumacher EH, Smith EE, Minoshima S. Dierences in Processing Spatial Information by Women and Men as Revealed by PET. Paper presented at the meeting of the Society for Neuroscience, 1994. [27] Lavadas E, Del Pesce M, Mangun GR, Gazzaniga MS. Variations in attentional bias of the disconnected cerebral hemispheres. Cognitive Neuropsychology 1994;11:57±74. [28] Levy J. Lateral specialization of the human brain: behavioral manifestations and possible evolutionary basis. In: Kiger JA, editor. The Biology of Behavior. Corvallis: Oregon State University, 1972.
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[29] Levy J. Cerebral lateralization and spatial ability. Behavior Genetics 1976;6:171±88. [30] Levy J. Lateral dierences in the human brain in cognition and behavioral control. In: Buser P, Rougeul-Buser A, editors. Cerebral Correlates of Conscious Experience. New York: North-Holland, 1978. [31] Polson MC, Friedman A. Task-sharing within and between hemispheres: a multiple-resources approach. Human Factors 1988;30:633±43. [32] Posner MI, Walker JA, Friedrich FJ, Rafal RD. How do the parietal lobes direct covert attention? Neuropsychologia 1987;25:135±45. [33] Rapcsak SZ, Cumino CR, Heilman KM. Attentional neglect. Neurology 1988;38:277±81. [34] Reuter-Lorenz PA, Kinsbourne M, Moscovitch M. Hemispheric control of spatial attention. Brain and Cognition 1990;12:240± 66. [35] Shaywitz BA, Shaywitz SE, Pugh KR, Constable RT, Skudlarski P, Fulbright RK, Bronen RA, Fletcher JM, Shankweller DP, Katz L, Gore JC. Sex dierences in the functional organization of the brain for language. Nature 1995;373:607±9. [36] Smith EE, Jonides J. Working memory: a view from neuroimaging. Cognitive Psychology 1997;33:5±42. [37] Smith EE, Jonides J, Koeppe RA. Dissociating verbal and spatial working memory using PET. Cerebral Cortex 1996;6:11± 20. [38] Springer SP, Deutsch G. Left Brain, Right Brain. New York: W. H. Freeman, 1993. [39] Wickens CD, Vidulich M, Sandry-Garza D. Principles of S-C-R compatibility with spatial and verbal tasks: the role of display± control location and voice-interactive display±control interfacing. Human Factors 1984;26(5):533±43. [40] Wickens CD, Mountford SJ, Schreiner W. Multiple resources, task-hemispheric integrity, and individual dierences in timesharing. Human Factors 1981;23(2):211±29.
www.elsevier.com/locate/neuropsychologia
Dierences in visual attention and task interference between males and females re¯ect dierences in brain laterality Heather Davidson a, Kyle R. Cave b,*, Daniela Sellner c a
Department of Psychology and Human Development, Vanderbilt University, Box 512-GPC, Nashville, TN 37203, USA b Department of Psychology, University of Southampton, High®eld, Southampton, SO17 1BJ, UK c Institut fuÈr Psychologie, 37073 UniversitaÈt CoÈttingen, Germany Received 16 February 1998; received in revised form 27 April 1999; accepted 4 May 1999
Abstract Two cognitive tasks (a letter memory task and a spatial memory task) designed to selectively activate the left or right hemisphere were combined with attentional probe tasks to measure how hemispheric activation aects attention to left and right hemi®elds. The probe task in Experiment 1 required the identi®cation of digits in the left and right hemi®eld. During the letter task, male subjects identi®ed more probes from the left hemi®eld than from the right. Their accuracy varied little across the two hemi®elds during the dots task. Experiment 2 tested whether this pattern is due to either spatial attention or interference in character processing. Instead of identifying digits, the probe task required subjects to respond to a black square that appeared in the periphery of the screen. For male subjects, the pattern was opposite of that from Experiment 1. During the letter task they responded faster to the probe in the right hemi®eld than in the left. Their response times were equivalent across the two hemi®elds during the dots task. These results indicate two separate eects of laterality in male subjects. The activation of one hemisphere produced more attention to the contralateral hemi®eld in Experiment 2, and the letter memory task interfered with the processing of other characters in the right visual ®eld more than those in the left visual ®eld in Experiment 1. Neither of these eects appeared in female subjects, corroborating earlier claims that female brains are less lateralized than male brains. # 2000 Elsevier Science Ltd. All rights reserved. Keywords: Visual selection; Character recognition; Hemispheres; Spatial probes; Sex dierences; Orienting
1. Introduction The early stages of visual processing in cortex are divided between the left and right hemispheres, with each hemisphere taking responsibility for the contralateral side of visual space. This study tests claims that functions of visual attention are also divided across the hemispheres, and also tests how attentional and other visual functions are in¯uenced by other brain processes occurring in the left and right hemispheres. * Corresponding author. Tel.: +44-2380-592234; fax: +44-2380594597. E-mail address: [email protected] (K.R. Cave).
Because previous studies have indicated dierences in brain laterality between male and female subjects, this study also tests for dierences in laterality between these two groups. 1.1. Evidence for hemispheric control of spatial attention Patients with visuo-spatial neglect are often described as having a de®cit in the ability to shift their attention towards the contralesional hemi®eld [32]. These de®cits suggest that each hemisphere may have a special role in controlling shifts of attention in the contralateral direction or to the contralateral side of space. Brain imaging studies show evidence of speci®c hemispheric activation during attention tasks in nor-
0028-3932/00/$ - see front matter # 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 0 2 8 - 3 9 3 2 ( 9 9 ) 0 0 0 8 4 - 6
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mal subjects. An experiment by Corbetta et al. [10] indicated that the superior parietal and superior frontal cortex were more active when attention was shifted in a peripheral direction than when attention was ®xated on the center of the visual ®eld. They found a correlation between the shifting of attention in the peripheral direction and activation of regions in the superior parietal lobe around the postcentral sulcus. Moreover, the magnitude of the activation in the contralateral hemisphere was twice as large as the activation in the ipsilateral hemisphere. Another piece of evidence that each hemisphere specializes in contralateral shifts of attention came from a study with split-brain patients by Lavadas et al. [27]. The subjects' heads were tilted 908 to the right or left to disassociate left and right visual ®elds from the left and right sides of their environment. Under these conditions, the right hemisphere demonstrated an advantage for detecting stimuli on the left side of environmental space, and the left hemisphere showed an advantage for the right side of environmental space. Each hemisphere apparently plays a special role in attending to the opposite side of space, even when it does not correspond to the contralateral visual ®eld. Reuter-Lorenz and Kinsbourne [34] presented behavioral evidence that each hemisphere has a special role in allocating attention in the contralateral direction in normal subjects. They hypothesized that when one hemisphere is more active than the other, attention can be biased in the direction contralateral to the more activated hemisphere. They assumed that if a visual stimulus is presented in the right visual ®eld, then the activation in the left hemisphere should increase, and the tendency to allocate attention in the rightward direction should increase as well. To test this activation orienting hypothesis, they presented subjects with a line bisection stimulus presented tachistoscopically in only one hemi®eld on each trial. In this task, the subject bisects a horizontal line by drawing a small vertical mark intersecting the line at its midpoint. The deviation between the actual midpoint and the subject's mark re¯ects the attentional bias. With neglect subjects, the deviation between the subjective and real midpoint is usually quite high. Reuter-Lorenz and Kinsbourne, however, tested normal subjects and found small but signi®cant deviations. If the stimulus was presented in the right visual ®eld (presumably activating the left hemisphere), the midpoint was drawn too far to the right, re¯ecting a left side underestimation. In other words, the right portion of the line was better attended than the left. They found the opposite eect when a visual stimulus was presented in the left visual ®eld, activating the right hemisphere. These results suggest that visual stimuli may contribute to the activation of a hemisphere, therefore promoting an attention shift in the contralateral direction.
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Reuter-Lorenz and Kinsbourne's results are consistent with Kinsbourne's [23,24] earlier claims that both hemispheres work simultaneously to shift attention in opposite directions. He characterized neglect not as an attentional de®cit but as an attentional bias toward one side resulting from an imbalance in the system that controls lateral shifts of attention. Although Kinsbourne's ®ndings have not always been successfully replicated [2], his theoretical claims have been in¯uential in the study of hemispheric interactions. Kinsbourne [23] proposed that in normal subjects each hemisphere generates tendencies to shift attention in the contralateral direction. A visual stimulus can activate attention centers in both hemispheres, and the internal inhibitory con¯ict between them causes a balance between the tendencies for the hemispheres to shift attention in opposite directions. When the tendencies are balanced precisely, attention falls naturally in the center of the stimulus. Kinsbourne [24] attributed the fact that left neglect appears more often than right to a more powerful rightward than leftward tendency to shift attention in normal subjects. Kinsbourne [23] suggested that each hemisphere controls contralateral shifts because visual stimuli processed in the cortex can trigger excitation of the ipsilateral superior colliculus. Each colliculus inhibits the other, which causes a mutual inhibitory balance between hemispheres. Damage to one hemisphere, such as in neglect, interferes with the excitatory inputs to the colliculus, disrupting the balance with the colliculus on the opposite side. Since the damaged hemisphere is inhibited, the undamaged hemisphere has less inhibition and produces a bias to shift attention in the contralateral direction. Therefore, the contralesional side of the visual ®eld is neglected. Reuter-Lorenz and Kinsbourne's results were just as predicted by the activation orienting hypothesis, but they might also be explained by more speci®c attentional interactions. Each stimulus was presented in only a single hemi®eld, in order to activate the contralateral hemisphere. When the stimulus appears alone in the left hemi®eld, for example, it will probably induce an attention shift to the left of the visual ®eld. This global attention shift might bias the subject to attend to the left side of the stimulus. In other words, the allocation of attention in a global context might bias attentional allocation in a local context, independently of the degree of neural activation within the left hemisphere. The experiments presented below tested whether other tasks that are performed primarily within one hemisphere or the other would bias spatial attention to visual stimuli that are equally balanced across both hemi®elds. Two tasks were chosen that have been shown by PET studies to activate the left or right hemisphere [19,36,37]. The left hemisphere was activated with a letter memory task, and the right
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hemisphere was activated with a spatial memory task. Neither task explicitly drew attention to either side of the visual ®eld. 1.2. Evidence for gender dierences in brain laterality There is evidence from a number of dierent sources that interactions between hemispheres vary between male and female subjects (see Hellige [13], Iaccino [18], and Springer and Deutsch [38] for reviews). Females tend to perform better on linguistic tests, including articulation speed, verbal ¯uency, grammar, and verbal production, while males tend to score higher on spatial tests, including mathematics, maze performance, and mental rotation [12]. Levy [28±30] suggested that females represent language in both hemispheres, which improves communication abilities but impairs spatial skills. Bryden [7] concluded that the left hemisphere is dominant for speech and that the right hemisphere is dominant for spatial tasks more often in right-handed males than in right-handed females. A variety of perceptual experiments have compared detection in the left and right visual ®elds by male and female subjects under dierent ®xation conditions. Although some studies ®nd no asymmetries in males, Iaccino [18] reviews many that have indicated an LVF advantage in males for nonverbal materials such as photographed faces, and RVF advantages for verbal materials, indicating a stronger lateralization of higher perceptual functions in males than in females. Dichotic listening studies have also indicated stronger lateralization of verbal processing in males [25], although in general the results from auditory lateralization experiments have been mixed and sometimes confusing. Hellige [13] summarizes reviews by Hiscock et al. [17] and Hiscock et al. [15,16] of 37 auditory, visual, and tactile tests. Twenty-®ve of the studies reviewed indicated greater laterality in males than females, which, as Hellige observes, is a statistically signi®cant proportion. Laterality dierences have also been found between males and females in measures of brain activity, although these ®ndings have also been mixed and sometime confusing. In one of the more recent studies, Shaywitz et al. [35] examined the brain activity in right-handed males and females during phonological tasks with functional MRI. They found that in males, brain activation was lateralized to the left inferior frontal gyrus. In females the pattern of activation was 1 Lauber et al. subsequently tested additional subjects in these tasks, but they were unable to replicate these dierences between male and female subjects (Lauber, personal communication). Whether or not these two types of tasks reliably produce dierent brain activations in males and females, the fact that they dierentially activate left and right hemispheres has been demonstrated in multiple experiments [19,36,37].
very dierent, engaging more diuse neural systems that involve both the left and the right inferior frontal gyrus. Dierences in brain lateralization between males and females was also found in a PET study by Lauber et al. [26] that included two tasks very similar to those used in the experiments presented below. In Lauber et al.'s study, a letter-memory task increased the activation in certain areas of the left hemisphere in male subjects. Each subject was shown a series of letters on a computer, presented one at a time. After each presentation the subject was asked if the current letter on the screen was the same letter as the letter three trials back. The case of the letters was varied to force matching by letter identity rather than shape. Male subjects showed a signi®cantly higher level of activation in the left hemisphere and no signi®cant right hemisphere activation in the frontal lobes. Both hemispheres were active in the female subjects. The stimulus in Lauber et al.'s spatial memory task consisted of a pattern of three dots in random locations around a ®xation cross. After the dots disappeared, the subject was presented a probe circle and asked to respond YES or NO, by pushing a button, indicating whether a dot had appeared in the circle's location. The male subjects had higher activation levels in the right hemisphere than in the left. The highest region of activity for males was right area six, followed by the right posterior parietal regions. The female subjects showed bilateral activation across both hemispheres during the spatial working memory task. In general, Lauber et al.'s ®ndings from the verbal and spatial tasks suggest that male subjects are more lateralized than female subjects for both tasks1. The asymmetries in brain activation demonstrated by Lauber et al. suggest that we can use these two working memory tasks to activate each hemisphere individually. However, the dierent patterns of activation between male and female subjects require that we examine the data from both groups separately. If Lauber et al.'s ®ndings do re¯ect a real dierence in cortical organization between males and females, then we can expect to ®nd lateralized attentional eects with these tasks only in the male subjects. In our experiments, each subject performed modi®ed versions of these letter memory and spatial memory tasks, each in a separate block of trials. Only data from right-handed subjects are presented here. On each trial the memory task was combined with a spatial probe task to measure the allocation of spatial attention while the letters or the dot locations were retained in working memory. In Experiment 1 the spatial probes were similar to the letter array used by Kim and Cave [20,22] and by Bichot et al. [1]. In Kim and Cave's ®rst experiment [20], a search array (an array of squares and circles) was presented brie¯y
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around a ®xation cross. The subject was then asked to press a button to indicate whether the target had appeared. Then a circular array of black letters was presented brie¯y. Using the mouse, subjects reported the letters they had seen in the display. Kim and Cave [22] and Bichot et al. used a similar procedure. In all of these studies, letters were more often correctly identi®ed when they were in the location previously occupied by a search target. In each trial of Experiment 1, subjects ®rst saw the primary (memory) task stimulus, either a letter or an array of dots, in the center of the display. Soon after it appeared, four digits appeared brie¯y in the periphery, two in the left hemi®eld and two in the right. Subjects reported all four digits, and then gave their response for the memory task. Based on Kim and Cave's results, we expect that dierences in the accuracy in reporting the probe digits will re¯ect dierences in spatial attention. We can test for lateralized attentional eects by comparing accuracy for left and right hemi®eld digit reports. 2. Experiment 1 2.1. Methods 2.1.1. Subjects Fifty-two male and ®fty-one female undergraduates from Vanderbilt University participated in this experiment. Only right-handed subjects were used. Each subject had normal or corrected to normal vision.
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The probe stimuli in both right and left hemisphere tasks consisted of four black digits, numbers 0 to 9, appearing for 30 ms. Each digit was in 22 point bold Monaco font. The four digits were each 7 mm tall and were placed in a square formation 87 mm on each side, so that each digit was 62 mm from ®xation. 2.1.4. Procedure The two dierent primary tasks were separated into two separate blocks of trials. Half of the subjects began with the left hemisphere (letters) task and the other with the right hemisphere (dots) task. In each block the subject viewed a series of displays. In each trial of the dots task, the subjects were instructed to keep their eyes ®xed on the ®xation cross throughout each trial (see the right side of Fig. 1). Two small red dots appeared on the middle of the screen for 180 ms. The locations of these red dots were dierent for each trial. As part of the primary task, the subject was asked to remember the locations of the dots on the screen. After the two dots disappeared, four digits appeared. The SOA (the delay between the onset of the primary stimulus, the dots, and the onset of the probe stimulus, the digits) was either 195, 240, or 285 ms. The digits were located farther in the periphery than the dots. As the subject continued to remember the position of the dots, he or she reported the digits using the mouse to mark the chosen digits on a list on
2.1.2. Apparatus Three Macintosh IIsi computers were used, each with a 13 inch Applecolor monitor and attached mouse. Subjects used a chin rest to keep them approximately 50 cm from the computer screen. 2.1.3. Stimuli A ®xation stimulus was present in the center of the display. For the dots task it was a cross, 4 mm wide and tall, and for the letters task it was a black box 13 mm wide and 18 mm high. The primary stimuli in the dots (right hemisphere) task consisted of two solid red dots with a diameter of 3 mm. The red dots appeared in dierent locations around a ®xation cross. There was at least 11 mm between every pair of dots and between each dot and the ®xation cross. The maximum distance between each dot and the ®xation cross was 28 mm. A green ring, 6 mm in diameter, appeared for the length of time it took the subject to respond to the primary task. The primary stimuli in the left hemisphere task consisted of an 11 mm red letter in 38 point bold Monaco font, either lower or upper case, that appeared in the box.
Fig. 1. These diagrams symbolize the sequence of displays for the two memory tasks in Experiment 1. See the text for the stimulus dimensions.
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the screen. Each subject was required to report all four digits on each trial, guessing if necessary. After the subject reported the digits, a small green circle appeared on the screen. The subject used the mouse to click a YES or NO box indicating if one of the red dots had been located within the position of the green circle. Following this presentation, a display appeared for 2 s, indicating which digits were reported correctly. The letters task was very similar to the dots task. Before the trials began, two letters were shown to the subject, one after another, to start the sequence of letters to be remembered. During each trial the subject was asked to ®xate on a black box (see the left side of Fig. 1). An upper or lower case letter appeared in the box for 180 ms. The subject's primary task was to decide whether that letter was the same letter as the letter that appeared two trials back, ignoring the case of the letter. Soon after the letter disappeared, four probe digits appeared, just as in the dots task. The SOA's between primary and probe stimuli for the letters task were the same three values used in the dots task. As the subjects retained the most recent letters in their memory, they were asked to identify the four digits, using the mouse. After reporting the digits and observing those which they answered correctly, the subject was asked to select with the mouse a YES or NO button indicating whether the letter presented on this trial matched the letter appearing two trials back. In both blocks of trials of this experiment the subjects were encouraged to take as much time as necessary to respond. Each block began with 15 trials of practice (more if the subject or experimenter thought it was necessary). Each block consisted of 72 trials (not including practice). The subjects were oered a break near the middle of each block.
analyses. In the letters task, one male subject and two female subjects produced more than 35% errors and in the dots task ®ve male subjects and twelve female subjects produced more than 35% errors. A total of ®ve male subjects and fourteen female subjects were discarded from the analysis. The data for males and females were analyzed separately. 2.2.2. Probe task The percentages of incorrect probe digit responses at each location were calculated separately for male and female subjects. These data were then analyzed to test whether the frequency with which subjects reported digits from the two sides of visual space varied between the two primary tasks. The probe accuracy data were submitted to fourway ANOVAs with dots or letters task, left or right hemi®eld, SOA, and upper and lower hemi®eld as factors. The analysis for the male subjects revealed a signi®cant interaction between hemi®eld and task (see Fig. 2), but the direction of the eect was opposite to what was expected. Males correctly reported fewer letters from the right hemi®eld than from the left during the letters task, and slightly fewer from the left hemi®eld than from the right during the dots task, F(1,44)=6.008, p < 0.05. Assuming that the two tasks activated the left and right hemispheres in the male subjects as in previous PET studies, then activating a hemisphere in this task produced better performance in the ipsilateral hemi®eld rather than the contralateral. The female subjects showed no hint of the interaction between memory task and probe hemi®eld that appeared in the male data, F < 1. In both tasks, the females reported slightly more digits in the right hemi®eld than the left (see Fig. 3). Unlike the males, the
2.1.5. Design The dependent variable in this experiment was the accuracy (percent error) for reporting digits at each location. Data from male and female subjects were analyzed separately. Each analysis included four factors: the primary task (dots or letters), probe digit hemi®eld (left of right), probe digit location within the hemi®eld (upper or lower), and SOA. 2.2. Results 2.2.1. Primary (memory) task The mean accuracy in the letters (left hemisphere) task was 86% for male subjects and 83% for female subjects. In the dots (right hemisphere) task, the mean accuracy for male subjects was 74% and for female subjects 71%. If any subject made more than 35% errors in either primary task, that subject's data were discarded from both right and left hemisphere task
Fig. 2. Error rates for identifying probe digits from the male subjects in Experiment 1.
H. Davidson et al. / Neuropsychologia 38 (2000) 508±519
Fig. 3. Error rates for identifying probe digits from the female subjects in Experiment 1.
females showed no evidence that these tasks produced dierences in visual processing across hemi®elds by activating one hemisphere more than the other. 2.2.3. Other signi®cant eects Both the male and female analyses showed several additional main eects and interactions. Male subjects made more mistakes in reporting probes during the letters task than the dots task, F(1,44)=15.1, p < 0.001, as did female subjects, F(1,36)=26.1, p < 0.001. Perhaps the letters task is generally more demanding than the dots task. However, the error rate of reporting the letters was lower than the error rate of reporting the dots. During both tasks, male subjects made more errors in reporting digits from the right hemi®eld than from the left, F(1,44)=4.4, p < 0.05. There was no main eect of hemi®eld in the female subjects; however, they reported slightly fewer digits correctly from the left hemi®eld than the right, F < 1. Fewer digits were reported from the lower hemi®eld than the upper, both for males, F(1,44)=23.4, p < 0.001, and females, F(1,36)=14.5, p < 0.001. This result may re¯ect an attentional bias to the upper hemi®eld. Some researchers have found that normal subjects will bisect a vertical line slightly above the midpoint [33], possibly indicating such a bias. For both male and female subjects, the dierence in performance between upper and lower ®eld probes was greater with the letters task than with the dots task; males: F(1,44)=4.4, p < 0.05; females: F(1,35)=10.8, p < 0.01. Probe error rates varied signi®cantly with SOA for both males, F(2,88)=7.3, p < 0.01, and females, F(2,72)=5.4, p < 0.01. For females, errors decreased as the time between the primary stimulus and the probes increased. For males, errors were highest for
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the shortest SOA and lowest for the intermediate SOA. For both males and females, however, varying the SOA only produced an overall dierence in error rate of 2 or 3%. For the female subjects there was a signi®cant interaction between SOA and probe hemi®eld, F(2,72)=3.3, p < 0.05. For the shortest and longest SOA's, responses were most accurate for probes on the right, but for the intermediate SOA they were slightly more accurate for those on the left. For each SOA, however, the dierence between the two hemi®elds was only 1 or 2%. There was no hint of such an interaction in the male data, F < 1. The male analysis also showed a four-way interaction between task, SOA, hemi®eld, and upper versus lower visual ®eld, F(2,88)=5.9, p < 0.01. For all three SOAs, the letters task produced more errors than the dots task, and these extra errors occurred mainly for digits on the right side rather than those on the left. However, the distribution of these extra errors across upper and lower visual ®elds diered with the SOA. In the shortest and longest SOAs (195 and 285 ms), the letters task produced many more errors for digits in the lower right quadrant, while for the middle SOA (240 ms) the extra errors associated with the letters task were distributed across the lower right, upper right, and lower left quadrants. No such interaction appeared in the females analysis, F < 1. Assuming that this interaction re¯ects a real dierence across SOAs, it does not appear to detract from attentional dierences between hemi®elds and the dierences between male and female subjects described earlier. 2.2.4. Comparing results across male and female subjects The data from both male and female subjects were combined in a single ANOVA to test whether the interaction of task and hemi®eld diered signi®cantly between the two subject groups. Although the dierences between the male and female data in Figs. 2 and 3 are rather striking, the three-way interaction between task, left versus right hemi®eld, and sex did not reach signi®cance, F(1,80)=2.1, p > 0.1. Although the interaction between these three factors was not signi®cant, these factors were part of a signi®cant ®ve-way interaction between task, SOA, left versus right hemi®eld, upper versus lower hemi®eld, and sex, F(2,160)=3.4, p < 0.05. From this, we concluded that the three-way interaction might vary according to the time between the primary stimulus and the digit probes. Therefore, each SOA was analyzed separately. The third SOA, 285 ms, did show a signi®cant three-way interaction between task, hemi®eld, and sex, F(1,80)=5.4, p = 0.023. For the ®rst two SOAs, 195 and 240 ms, the three-way interaction between dots or letters task, left versus right hemi®eld, and sex was not
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Table 1 Percentage of digit probes reported correctly in Experiment 1
Female verbal Female spatial Male verbal Male spatial
195 ms SOA Left probes
Right probes
240 ms SOA Left probes
Right probes
285 ms SOA Left probes
Right probes
34 30 32 31
33 26 37 29
32 28 31 28
33 28 33 29
33 26 30 28
29 25 36 28
signi®cant, although the trend was in the same direction. The probe data are presented separately for these three SOAs in Table 1. Apparently the nature of the primary task does aect males and females dierently, but the dierences appear most strongly after subjects have had time to become engaged in the primary task. This analysis produced no other signi®cant interactions including sex as a factor. 2.3. Discussion The two primary tasks aected the processing of left and right ®eld stimuli dierently in male subjects, but not in females, as expected. However, we expected lower accuracy for digits reported in the hemi®eld ipsilateral to the activated hemisphere in males, but instead accuracy was lower for the contralateral hemi®eld. This pattern seems quite stable, because we found similar trends in two other slightly dierent versions of the experiments2. There are three possible explanations for these dierences: the tasks employed to activate the hemispheres may have been interfering with attentional mechanisms rather than activating them, the tasks may have been interfering with mechanisms in each hemisphere that process characters, or subjects may be more likely to miss digits in the right hemi®eld when the error rate is high. According to the ®rst explanation, the primary tasks were successful in activating particular mech2 The two previous experiments varied from the present study in certain details of the tasks. In the ®rst experiment the displays for the spatial memory task consisted of three dots rather than two, which resulted in very low accuracy rates for the spatial memory task. With such a dicult dots task, subjects may not have been able to perform the probe task well enough to give good measures of spatial attention. In the second experiment, subjects were instructed to report two probe digits on each trial rather than four. In this case, subjects performed the probe task too well. Accuracy was so high that the probe data yielded less information about the allocation of attention. Despite the problems with these earlier experiments, the results from each were similar to those of the ®nal experiment. In both earlier experiments, males showed similar trends toward an interaction between memory task and probe hemi®eld, although it did not achieve signi®cance in either. The female data for one experiment showed a weaker trend in the same direction, and in the other showed a weak trend in the opposite direction.
anisms in the target hemispheres, and they pulled resources away from the attentional mechanisms in the same hemisphere. For example, during the letters task in male subjects, the letter stimuli activated the left hemisphere's areas for identifying and remembering sequences of characters, and this activation drew resources away from the attention mechanism in the left hemisphere. If Kinsbourne's [23] theory of hemispheric balance is correct, lack of activation in the left hemisphere would disrupt the balance, causing the attentional mechanisms in the right hemisphere to dominate and shifting attention contralaterally. Therefore, more digits would be attended in the left hemispace than in the right during a letter task. The second possible explanation does not involve spatial attention, but interference between two tasks relying on the same left-hemisphere resources [6,11,31,39,40]. Both hemispheres may have mechanisms for identifying and remembering characters, but the left hemisphere's mechanisms may be more developed because of its specialization for language. The idea of a single mechanism for recognizing both letters and digits is consistent with conclusions from Boles [3±5] based on factor analyses of the dierences in lateralization across subjects in a wide range of cognitive tasks. Based on his ®ndings, Boles composed a list of general cognitive functions, and claimed that each general function would vary in lateralization from subject to subject independently of other functions. Interestingly, Boles proposed a single cognitive mechanism for all visual lexical tasks, including both those involving letter stimuli and those involving digit recognition. Boles suggests that visual lexical processing is more strongly associated with the left hemisphere, so it is no surprise that our letters task might be performed primarily in the left hemisphere, limiting that hemisphere's ability to identify digits appearing in the right hemi®eld. Our dots task seems to ®t best with Boles' spatial positional function, which is independent of the visual lexical function and is typically associated with the right hemisphere. This hypothesis may explain why both male and female subjects reported more digits overall during the dots task than during the letters task, because brain mechanisms used to remember the
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dots will be less likely to interfere with those involved with processing the digits. A ®nal explanation arises from the observation that the letters task interfered more with digit reports than the dots task. When subjects are limited in the number of digits they can report, they may be more likely to report those on the left because of habits developed in reading. This explanation predicts a similar left hemi®eld advantage if the dots task is made more dicult. In a previous experiment described in footnote 2, we did use a more dicult dots task. In this experiment, the probe error rate with the dots task was similar to that in the letters task, but in the male subjects there was still no left hemi®eld advantage with the dots as there was with the letters. Thus, the results from the preliminary experiment argue against this alternative explanation. Furthermore, it is dicult to see why this `start from the left' strategy would be limited to males. 3. Experiment 2 Experiment 2 was designed to distinguish between the two possible explanations for Experiment 1. The digit probes were replaced with a single dot probe, as used by Kim and Cave [20], Cave and Zimmerman [8], Cepeda et al. [9] and Kim and Cave [21]. Soon after the primary stimulus, a small square probe stimulus appeared at a single location on half the trials. When subjects detected the probe, they pressed a button as quickly as possible. Dierences in response time to dot probes at dierent locations re¯ect dierences in spatial attention. The dot probe provides a second attentional measure, and unlike the digit probes, it will not be susceptible to interference in character recognition. If the ®rst (attentional) explanation for Experiment 1's results is correct, then the probe RT's in Experiment 2 should show a similar advantage for locations ipsilateral to the activation from the primary task.
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3.1.2. Apparatus As in Experiment 1, three Macintosh IIsi computers, each with a 13 inch Applecolor monitor and attached mouse were used. Subjects used a chin rest to keep them approximately 58 cm from the computer screen. A response box connected to the computer had two buttons on the left labeled YES and NO, and one button on the right labeled BLACK SQUARE. 3.1.3. Stimuli The primary stimuli were identical to those in Experiment 1. The probe was a black square 3 mm on each side. When it appeared, it was 87 mm from ®xation at one of the four corners of an imaginary square around ®xation. 3.1.4. Procedure The primary tasks were identical to those in Experiment 1. Each primary stimulus was visible for 75 ms. Half of the subjects started with the letter task ®rst, the other half with the dots task. Instead of digit identi®cation, the subjects were required to respond as quickly as possible to the black square that ¯ashed in the periphery of the screen on half of the trials. The SOA [the delay between the onset of the primary stimulus (the letter or dots) and the onset of the probe stimulus (the black square)] was either 90, 135, or 180 ms, and the probe was visible for 30 ms. The subjects were asked to press a button on the response box as soon as the black square appeared (see Fig. 4). The same button was pressed regardless of the probe's lo-
3.1. Methods The attentional probe task in Experiment 2 did not require character processing. The probe was a black square, and the dependent variable was the response time for detecting the black square. This new probe task allowed the measurement of spatial attention while avoiding the possibility of interference in identifying and remembering characters. 3.1.1. Subjects Forty-four female and twenty-nine male undergraduates of the Vanderbilt University participated in the experiment. All were right-handed and each subject had normal or corrected to normal vision.
Fig. 4. These diagrams symbolize the sequence of displays for the two memory tasks in Experiment 2. See the text for the stimulus dimensions.
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cation. Each trial block began with at least 15 trials of practice. Each block consisted of 192 trials. The subjects were oered two breaks during the experiment. 3.1.5. Design The dependent variable in this experiment was the response time to the probe. Data from male and female subjects were analyzed separately. Each analysis included the same four factors as the analyses in Experiment 1.
3.2. Results The analysis for Experiment 2 was similar to that for Experiment 1. 3.2.1. Primary task The mean accuracy in the letters (left hemisphere) task was 92% for male subjects and 91% for female subjects. In the dots (right hemisphere) task, the mean accuracy for male subjects was 95% and for female subjects was 92%. Data from subjects who scored less than 65% correct in either primary task were discarded from both right and left hemisphere probe analyses. A total of three male subjects and ®ve female subjects were discarded from the analysis. 3.2.2. Probe task Every subject was at least 65% accurate on the probe task. The male analysis revealed a signi®cant interaction between left versus right hemi®eld and primary task F(1,28)=10.0, p < 0.01, and this time it was in the direction predicted by the activation orientation hypothesis. Males subjects responded faster to the probes in the right hemi®eld than to the left hemi®eld
Fig. 5. Response times for detecting probes from the male subjects in Experiment 2.
during the letters task (see Fig. 5), while left and right response times were almost equal for the dots task. The female subjects showed no hint of this type of interaction between primary task and left versus right hemi®eld, F(1,43)=1.4, p < 0.2. In both tasks, the females responded faster to the probe appearing in the right hemi®eld than the left (see Fig. 6). In fact, what trend there is in the female data is in the opposite direction from the male interaction. 3.2.3. Other signi®cant eects Both male and female subjects were generally faster in their probe responses during the dots task than during the letters task; F(1,43)=16.1, p < 0.001 for females and F(1,28)=30.0, p < 0.001 for males. As in Experiment 1, the spatial memory task seems to be less demanding than the verbal memory task. Responses were generally faster for probes on the right than on the left; F(1,43)=32.7 p < 0.001 for females and F(1,28)=15.2, p < 0.001 for males. Male subjects were faster for probes in the upper visual ®eld than in the lower visual ®eld, but only during the letters task and not during the dots task, F(1,28)=12.2, p < 0.01. Female subjects showed no signi®cant dierences between upper and lower visual ®elds. Probe response times varied across the three dierent SOAs in females F(2,86)=8.2, p < 0.001, but not in male subjects. The response time for females was longer for the fastest probes (90 ms SOA) than for probes that appeared later. 3.2.4. Comparing results across male and female subjects As in Experiment 1, another analysis combined the data of male and female subjects together. The threeway interaction between task, hemi®eld and sex was
Fig. 6. Response times for detecting probes from the female subjects in Experiment 2.
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signi®cant, F(1,71)=10.6, p < 0.01, emphasizing the dierence between males and females in the way that attention is aected by the two primary tasks. Other eects were consistent with what was seen in the male and female analyses. The way in which the two primary tasks aected probes in the upper and lower visual ®elds diered signi®cantly between males and females, F(1,71)=11.4, p < 0.01. There were no other signi®cant eects involving subject gender. 3.2.5. Probe errors The mean probe error rate was below 5% for both male and female subjects. Analyses of the probe response errors revealed no hint of a speed accuracy trade-o that would raise doubts about the conclusions from the response time data. The male subjects produced no signi®cant main eects or interactions. Female subjects made more errors during the verbal task in the lower visual ®eld and more errors during the spatial task in the upper visual ®eld, F(1,43)=5.5, p < 0.05. 3.3. Discussion The second experiment was designed to determine if the results of Experiment 1 were due to character processing interference or attentional interference. The results revealed an interaction of task and hemi®eld that was opposite to that in Experiment 1. The task that was designed to activate the left hemisphere in males increased attention to the contralateral hemi®eld. The pattern in Experiment 2 suggests that the activation of areas within one hemisphere can facilitate attention to the contralateral hemi®eld as originally predicted, and thus the results from Experiment 1 can be attributed to interference of character processing rather than attentional interference. This account of the dierence between the probe tasks seems plausible in light of Bole's [5] results when he used a task somewhat similar to our dots probe task. Boles reported only weak evidence of lateralization of this task in the left hemisphere, and no evidence that it correlated with the visual lexical or spatial positional functions. Therefore, Boles' prediction would probably be consistent with our results showing that the dots probe task does not interfere much with either the letters or dots task. The pattern of response times in Fig. 5 seems to show that the letter (left hemisphere) task produces an attentional advantage for the right hemi®eld over the left, while the dots (right hemisphere) task has no eect on attention. However, there may be a main eect that speeds responses to all probes on the right side relative to those on the left, which could cancel out the attentional eect of the dots task. Thus, while we cannot be certain of the details of the interactions between these tasks and spatial attention, we can be
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con®dent that these two tasks aect attention to the left and right hemi®elds in very dierent ways. 4. General discussion The two tasks in these experiments demonstrate both facilitation and interference between dierent processes within a hemisphere. Experiment 1 showed that in male subjects the identi®cation and memory of letters for the verbal task interfered with the identi®cation and memory of digits in the left hemisphere, as illustrated in Fig. 7. The results of Experiment 2 revealed that the activation of left hemisphere areas in male subjects during the verbal task facilitated the attention mechanism in that hemisphere, as illustrated in Fig. 8. Attention was shifted to the contralateral hemi®eld and caused a shorter probe response time in that hemi®eld. Previous studies have shown both hemispheric facilitation and interference as well. For example, Hellige and Cox [14] found that remembering a short list of nouns could facilitate visual recognition of right hemi®eld stimuli, while remembering a longer list interfered with right hemi®eld recognition. These two eects provide new insights to two dierent aspects of visual perception and its implementation in the brain. The facilitation in Experiment 2 serves as new evidence for the idea that attentional mechanisms in the two hemispheres compete to pull attention in opposite directions. It also shows that the allocation of attention to one set of stimuli is aected by other brain processes that are triggered by unrelated tasks with unrelated stimuli. The pattern of interference in Experiment 1 suggests that in male subjects a task that
Fig. 7. Hemispheric interactions during Experiment 1.
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Acknowledgements Thanks to Narcisse Bichot, William Caul, Carolyn Backer Cave, Min-Shik Kim, Erick Lauber, Patricia Reuter-Lorenz, Je Schall, Amy Shelton, Ed Smith, and Ken Sobel for comments. Thanks also to Paul Russell and Tom Birkett for providing software to control the Macintosh response keys and a design for the response key interface, and to Lonny Shimp for building the response keys. This work was supported in part by Grant P30-EY08126 from NEI awarded to the Vanderbilt Vision Research Center. References
Fig. 8. Hemispheric interactions during Experiment 2.
requires identifying and remembering letters will be assigned to the left hemisphere, where it will interfere with processing of other characters in the right visual ®eld more than those in the left. Although the eects in the two experiments were in opposite directions, they were similar in that female subjects showed no hint of interaction between task and hemi®eld in either experiment. Together these experiments provide two new pieces of evidence that there are basic dierences between male and female subjects in the performance of perceptual and cognitive tasks. The similarity in performance across hemi®elds in females may occur because female brains, or at least the mechanisms responsible for these tasks, are less lateralized than male brains. Therefore, the tasks did not exclusively activate one hemisphere in the female subjects, but rather activated both hemispheres, and the attentional mechanisms in both hemispheres were activated more or less equally. These results have implications for at least three dierent areas of research. First, they demonstrate new aspects of the division of attentional control across hemispheres. They demonstrate that control of attention is at least somewhat in¯uenced by other unrelated brain events, and that these in¯uences can result in attentional dierences between men and women. Second, they provide new evidence on how the work of processing symbolic characters is distributed across the cortex. Third, they illustrate two new perceptual tasks for studying laterality dierences between males and females. These dierences have been elusive and dicult to pin down in the past, and these new experimental methods should help to determine what dierences there are in brain organization and how these dierences aect perceptual and cognitive processing.
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