Section of Visual Science, University Eye Clinic, Waldhoernlestrasse 22, D-72072 Tuebingen,
1 University Hospital of Psychiatry and Psychotherapy, Osianderstrasse 24, D-72076 Tuebingen and
2 Institute for Brain Research IV, Human Neurobiology, Centre for Cognitive Sciences, Argonnenstrasse 3, D-28211 Bremen, Germany
Received 5 August 1999; in revised form 8 November 2000; accepted 10 November 2000
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ABSTRACT |
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INTRODUCTION |
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On the other hand, alcoholism is known to impair performance in a variety of cognitive functions as assessed by clinical neuropsychological tests. These neuropsychological deficits are often summarized as showing a more severe deficit in visualspatial than in verbal functions (e.g. Butters et al., 1977; Ryan and Butters, 1980b; Leber et al., 1981; Becker et al., 1983; Donat, 1986; Tarbox et al., 1986; Reed et al., 1992; Fabian et al., 1994). However, most clinical tasks testing visual functions such as visual short-term memory are often not restricted to the visual domain. Mostly, they consist of material, such as geometric configurations or pictures to be remembered or reproduced by the subjects (Ryan and Butters, 1980b; Leber et al., 1981
; Becker et al., 1983
; Brandt et al., 1983
; Donat, 1986
; Tarbox et al., 1986
; Arria et al., 1991
; Reed et al., 1992
; Zhang et al., 1997
). Therefore, these configurations can often be encoded not only visually, but also verbally, and performance in these tests depends not only on visual memory, but also on the use of, e.g. semantic coping strategies.
In the present study, we assessed basic visual functions in recently detoxified patients with chronic alcohol misuse by means of psychophysical tasks. These tasks are designed to test specific visual functions, thereby limiting coping strategies. The aim of this study was to assess the impact of chronic alcohol misuse on basic visual functions such as motion perception, visual short-term memory and visual divided attention. The following is a background summary of these three tasks.
In the first task, we assessed visual short-term memory in recently detoxified patients and a matched control group by means of a delayed vernier discrimination task. In this test, the discriminative feature of the stimulus, namely the offset of a vernier, can be encoded only visually, thus limiting the use of coping strategies. This psychophysical task in contrast to the Benton Visual Retention Test has been demonstrated to be sensitive to the deficits in visual short-term memory during moderate acute intoxication (Wegner and Fahle, 1999).
The second task applied in the present study addressed two aspects of visual motion perception by adapting the paradigms of Newsome and Paré (1988) and Sekuler (1990): speed discrimination and integration of local motion signals in the presence of stimulus noise. These tests are considered to be a sensitive measure of the function of an extrastriate cortical area lying medial temporal (MT), which contributes to the visual perception of motion (Dubner and Zeki, 1971; Zeki, 1974
; Maunsell and Van Essen, 1983
; Newsome and Paré, 1988
). A separate study applying the same tests in acutely intoxicated healthy volunteers (M. Fahle and A.-J.Wegner, in preparation) revealed that speed discrimination was significantly impaired during acute intoxication. In addition, alcohol differentially influenced visual motion perception depending on stimulus speed. These results indicated that alcohol selectively affected the integration of local motion signals for slow (2°/s) but not for faster (10°/s) speeds. This finding can be interpreted within the framework of the concept of two processing streams in visual motion perception. In the present study, applying the same stimuli, we investigated whether motion perception is affected by alcoholism and whether the selectivity in deficits observed in intoxicated healthy subjects may be found also in detoxified patients with chronic alcohol misuse.
The third task examined divided visual attention, more specifically, the processing of hierarchical letters, i.e. global letters composed of small local letters. Like the other tasks, this test is also confined to the visual domain, as attention has to be divided between two aspects of one visual stimulus. Since these stimuli have been demonstrated to reveal differential deficiencies in neurological patients, depending on the localization of the cortical lesions (e.g. Robertson and Lamb, 1991), this task can be utilized to test the hypothesis of lateralized cortical impairments in chronic alcoholism.
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MATERIALS AND METHODS |
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Potential participants, patients and controls, were screened using structured questionnaires, including assessment of general demographic information, history and quantities of alcohol consumption, family history of alcoholism or other psychiatric diseases, other drug-taking behaviour (medication, drugs, nicotine), and previously or ever experienced signs of withdrawal.
Patients were included in the present study if they fulfilled the following criteria: diagnosis of alcohol dependence/misuse according to DSM IV (American Psychiatric Association, 1994) and ICD-10 (World Health Organization, 1992
), normal or corrected to normal visual acuity, no psychiatric medication during hospitalization (including benzodiazepines), no psychiatric or neurological disorder, and alcohol misuse maintained until hospitalization (in order to assure that all patients were tested within their first week of detoxification), but no current blood alcohol. Patients receiving any psychiatric medication during the first week of detoxification such as benzodiazepines were excluded from the study. Moreover, patients with known histories of withdrawal complications and/or current serious signs of withdrawal were also excluded.
Control subjects with normal or corrected to normal visual acuity and no report of current or past history of alcoholism, neurological and/or psychiatric disease or medication were included. Alcohol-related data of patients and controls are shown in Table 1.
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Tasks
Visual acuity.
This was assessed by means of the Freiburg Visual Acuity Test. From a distance of 2 m, subjects have to indicate the orientation of Landolt-Cs of varying size (Bach, 1995).
Visual motion perception.
This was tested by means of random dot kinematograms (Newsome and Paré, 1988). Stimuli were produced with a Silicon Graphics computer Indigo® and consisted of 100 dark (4 cd/m2) dots with a dot size of 8 arcmin randomly distributed on a bright background (80 cd/m2) covering an area of 6 x 6 deg2 (i.e. 2.8 dots/deg2). Dots were refreshed every second frame (i.e. every 28 ms). At a viewing distance of 60 cm, all stimuli were presented centrally for 200 ms. No fixation point was provided.
The first test assessed the ability to integrate local motion signals in the presence of motion direction noise. Dot speed was constant at either 2°/s or 10°/s, varied between blocks. The subjects' task was to report the direction of the coherently moving dots with four directions being possible: up, down, left, or right (four alternative forced choice: 4AFC). The dots constituting the motion direction noise were randomly replaced (Fig. 1).
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For the second test, a speed discrimination paradigm, the random dot kinematogram comprised a horizontal row (stripe), 1° high, extending over the total width of the stimulus. The stripe was defined by dots moving at a slightly higher speed than the surrounding dots and was located 1° from either the upper or lower border of the stimulus (Sekuler, 1990). All dots moved either in one direction, i.e. to the left or right (unidirectional stimulus) or else half of the dots moved to the right, whereas the other half moved to the left (bidirectional stimulus). Unidirectional and bidirectional conditions were tested in separate blocks for a fixed base speed of 10°/s (Fig. 2
). The subjects' task was to report whether the stripe was in the upper or the lower part of the random dot kinematogram (two alternative forced choice: 2AFC). For the determination of thresholds, the speed difference was varied according to the adaptive staircase procedure (PEST).
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Biasing. The frequency of the target letters appearing on both target levels (global or local) was manipulated, yielding three conditions: In the no bias condition, target letters (H or S) were equally often presented on the global and local level. In the global bias condition, 75% of the target letters appeared on the global level, whereas in the local bias condition, 75% of the target letters were presented on the local level.
Bias conditions were measured in three separate blocks of 64 presentations each. The order of bias conditions was either local biasno biasglobal bias or global biasno biaslocal bias, randomized between subjects. Subjects were not informed about biasing.
Distractor effect.
In the present study, H and S were the target letters and A and E served as distractors. These letters were chosen since A is similar to H but less than to S, whereas E is similar to S but less than to H. Thus, for each target letter, there exists one similar (HA; SE) and one dissimilar (SA; HE) distractor letter (Robertson et al., 1988; Lamb et al., 1990
; Giersch et al., 1997
). The distractor effect refers to the observation that reaction times to local targets were faster if the local target letters (H or S) compose a similar global distractor letter (A or E). Classically there is no such effect for global target letters.
Visual short-term memory: delayed vernier discrimination
This test assesses visual short-term memory using very simple visual stimuli, i.e. verniers (Fahle and Harris, 1992). The vernier target consisted of two vertical lines, each 50 arc min long and 2 arc min wide with a 0.5 arc min vertical gap between them. The lower segment was always displaced to the right by either 580, 620 or 740 arc s. The first vernier was presented for 100 ms on an analogue monitor under computer control. After a delay of 1 s, a second vernier with either a smaller or a larger offset was presented for 100 ms at about the same position as the first (Fig. 4
).
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Thresholds were determined by the adaptive staircase procedure (PEST), i.e. test stimuli became more similar and therefore harder to discriminate as long as subjects' answers were correct. On the other hand, a level answer led the staircase procedure to present more easily distinguishable stimuli. This adaptive procedure converged to a stimulus configuration yielding 75% correct responses, which is taken as the subjects' discrimination threshold.
Initial orientation of the stimulus was either horizontal or vertical, counterbalanced between observers. For the second session, the orientation of the vernier was changed by 90°. Previous studies (Poggio et al., 1992) have shown that changing the orientation of the vernier by 90° prevents transfer of improvement to the new orientation.
Analysis
For the data of the visual acuity, motion, and visual short-term tasks, a repeated measurements analysis of variance (ANOVA) was calculated using group (patientscontrols) as between subjects factor, and session (firstsecond testing) as within factor. For the divided attention task data, a repeated measurement ANOVA, with group (patientsnormals) as between factor and session (firstsecond testing), target level (localglobal), bias condition (global bias, local bias, and no bias), and distractor similarity (similar dissimilar) as within factors was calculated. In addition, we correlated RTs and error data in order to detect possible speed accuracy trade-offs, i.e. a decrease in RTs at the expense of the error rate.
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RESULTS |
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Integration of local motion
For the slow speed tested (2°/s), alcoholic patients required significantly higher coherence thresholds (%) than normal controls, both in the first and the second sessions (P = 0.0022 and P = 0.16, respectively; Fig. 5). Neither group significantly improved in the second examination (both P > 0.2).
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Speed discrimination
For the unidirectional stimuli, patients' thresholds were significantly elevated as compared to those of normal controls, both in the first and the second session (P = 0.005 and P = 0.01, respectively; Fig. 6). The patients, but not the normal controls, significantly improved in the second session (P = 0.03 versus P > 0.1, respectively).
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Divided attention
Overall reaction times did not differ between normal controls and patients (P > 0.4). Thus patients did not show a significant overall increase in reaction times. However, during the second session, both groups reacted faster by an average of 50 ms (both P = 0.001).
Neither patients nor controls demonstrated a speed accuracy trade-off indicative of a strategy favouring either speed at the expense of accuracy or vice versa. [These results are in accordance with findings of Glenn and Parsons (1991) who reported a similar speedaccuracy relationship both in alcoholic patients and controls if both factors were emphasized in the task instructions.]
Error rates were significantly higher in patients than in controls, only for the first examination (P < 0.0001 and P > 0.3 in the first and second session, respectively). Patients, but not controls, yielded significantly lower error rates in the second examination (P < 0.0001 versus P = 0.17). However, mean error rates were low (3.7% ± 0.3 and 5.1% ± 0.4 in controls and patients, respectively).
Biasing
Both in controls and patients, we found a significant bias effect (both P < 0.0001), i.e. a faster reaction to the more often presented target level (Fig. 7). In the local bias condition with 75% of the targets presented on the local level, both groups reacted faster to the local, i.e. biased, level. Similarly, in the global bias condition, subjects reacted faster to global targets. Finally, in the no bias condition with equal probability of both target levels, subjects had similar RTs to both levels (Fig. 7
).
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Distractor effect
The similarity of the distractor affected the RTs to local targets, i.e. subjects reacted faster to local targets with similar distractors than with dissimilar distractors (target level x similarity: P = 0.03 and P = 0.0026 in normal controls and patients, respectively) (Fig. 8). The interactions of target level x similarity x session and target level x similarity x group were not significant, indicating that the distractor effect did not differ between examinations or groups (Fig. 8
).
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DISCUSSION |
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A region lying medially in the temporal cortex (MT) is thought to play a major role in the perception of coherent motion, i.e. the integration of local motion signals. The visual system seems to process motion by at least two streams which are specialized for different speeds: one pathway for slow motion, derived from the parvocellular layers of the lateral geniculate nucleus (LGN), which sequentially projects to the primary visual cortex (V1) and the prestriate cortex, including MT; and a second pathway, stemming from the magnocellular layers of the LGN, which projects to V1, MT, and other prestriate areas in parallel rather than sequentially. This pathway becomes dominant for speeds exceeding about 6°/s (ffytche et al., 1995).
Since we found a significant impairment for the slower, but not the faster, speed tested, we assume that both acute alcohol intoxication and chronic alcoholism mainly affect the sequential processing stream from the LGN via V1 to MT, but not the direct projection to MT which is predominantly active during the processing of faster speeds.
Speed discrimination
Thresholds in the bidirectional condition were higher than those in the unidirectional condition. According to Sekuler (1990), this difference in thresholds reflects differences in the processing between both kinds of stimuli: whereas in the unidirectional condition, the position of the stripe can be detected by comparison of relative dot positions over time, i.e. by positional cues, speed discrimination is more difficult in the bidirectional condition, since there are no positional cues, and speed information has to be extracted across different directions in order to determine the position of the stripe.
Patients were impaired in the discrimination of speed differences, when compared to normal controls. This impairment was significant only for unidirectional, but not for bidirectional, stimuli. Thus, in the easier task, patients showed deficiencies, whereas they performed as well as controls in the more difficult speed discrimination task. These results reflect the fact that the normal controls were quite good in the unidirectional speed discrimination task, but yielded elevated thresholds in the bidirectional stimuli when shown for the first time (see Recovery of speed discrimination below).
Divided attention
Robertson and Lamb (1991) proposed a model composed of four subsystems for the processing of hierarchical stimuli, suggesting that the global level of the stimulus is predominantly processed in the right posterior superior temporo-parietal regions, whereas the local level is mainly processed in its left counterpart. Damage to one of these regions causes RT advantages for one level at the expense of the other target level. A third subsystem controls attention, as assessed, e.g. by the biasing paradigm, and is thought to be associated with the lateral parietal lobes of both hemispheres, while the fourth combines information from both hemispheres. Thus, one might assume that distractor effects rely on the normal (asymmetric) coordination of the information from both hemispheres, resulting in global or local interference. In responding to these hierarchical letters, patients were not impaired in overall RTs, as compared to normal controls matched for age and education. Thus, chronic alcohol misuse does not seem to slow overall processing and reaction to visual stimuli.
However, during the first session, error rates were increased in patients, but decreased to levels reached by control subjects during the second examination. Thus, attentional capacities seemed to be only initially impaired in patients during early detoxification as indicated by elevated error rates, but to recover within 3 weeks of abstinence. These results are in contrast to the study by Smith and Oscar-Berman (1992) reporting decreased attentional and/or perceptual resources in patients even after more than 4 weeks of abstinence. The discrepancy may be due to a shorter period of alcohol misuse reported by the patients in the present study, i.e. 7.13 years in the present as compared to 23 years in the above study, which would be expected to have less severe consequences (e.g. Butters et al., 1977; Ryan and Butters, 1980a) with shorter lasting attentional deficits.
Attentional allocation: biasing paradigm
If the target letter is more often presented on one than on the other level of the hierarchical stimulus, i.e. during biased presentation, RTs to the biased level decrease, whereas RTs to the unbiased level slightly increase as compared to the no bias condition (biasing effect). This effect may be explained by attentional allocation: the reaction to the more frequently presented target level is faster due to a shift in attention to the biased level, at the expense of the less-often presented target level. Allocation of attention, as assessed by the present biasing paradigm, was not adversely affected in detoxified patients with chronic alcohol misuse. As in normal controls, RTs of patients to the biased level were faster than to the non-biased target level. In addition, RTs to the local and global target levels were about equal in the no bias condition, i.e. with equal probability of both target levels.
These results seem to contradict the findings of Robertson et al. (1985) and Kramer et al. (1989), who reported a preference of alcoholic patients to attending to the local, rather than to the global, level. However, in the Robertson et al. (1985) and Kramer et al. (1989) studies, there existed no correct or incorrect reactions, only subjective judgements based on either the local or global level of the stimulus, and patients had longer histories of alcohol misuse. Hence, there may be a spontaneous preference for the local level, but, on demand, patients can shift attention between levels as well as do normal controls.
Cortical hemispheres do not seem to be asymmetrically affected in alcoholism, since alcoholic patients, like controls, yielded similar RTs to both the local and global target levels in the no bias condition. In addition, patients demonstrated a normal pattern during biasing, with no overall preference for the local level, as would be expected on the basis of the right hemisphere theory of alcoholism. Moreover, the distractor effect was slightly enhanced in patients (see below), indicating that local processing seems to be even more affected by the similarity of the global distractor than in controls. If one assumes, on the other hand, a deficient global processing due to right hemispheric impairments, the distractor effect should be diminished or even abolished, since the global pattern should no longer influence the local judgement.
Interference: distractor effect
The classical distractor effect observed with hierarchical letters implies that the processing of the local, but not the global, target level is affected by the similarity of the distractor letter: if the global distractor is similar to the local target letter, RTs are faster than with a dissimilar distractor. In the present study, this kind of interference was quite similar both in normal controls and patients. The distractor effect is thought to be mediated by the (asymmetric) combination of information from both hemispheres and is probably processed in both posterior temporal areas (Robertson and Lamb, 1991). Thus, the qualitatively normal distractor effect in patients indicates a normal coordination of global and local information from both hemispheres. However, the small quantitative differences observed in recently detoxified patients may indicate a larger than normal influence of global information, processed in the right hemisphere, on local processing in the left hemisphere during the early phase, i.e. the first days of detoxification, opposite to the predictions by the theory of right hemispheric deficits in alcoholism (see also below).
Visual short-term memory
This psychophysical task, restricted to visual encoding, thereby preventing semantic coping strategies, was very sensitive in revealing visual short-term memory loss during acute alcohol intoxication (Wegner and Fahle, 1999), i.e. intoxicated healthy subjects yielded significantly elevated thresholds as compared to sober subjects. These results are at variance with the present findings in patients demonstrating no significant impairments, as compared to normal controls. Comparisons with reference thresholds determined for the same task (Fahle and Harris, 1992
; Wegner and Fahle, 1999
) indicated that thresholds of the normal controls in the present study were higher than usually observed, especially in the first examination, and thus not significantly different from those of patients. A correlation between discrimination thresholds and subjects' age revealed no systematic change in thresholds with age, neither in patients, nor controls (P > 0.7 and P > 0.1, respectively), excluding an explanation based on age differences.
Recovery of visual motion perception
In order to detect potential recovery of visual functions during the first weeks of detoxification, patients were retested after 3 weeks of controlled abstinence. To account for possible learning effects, controls were also retested 3 weeks later. For both speeds tested, patients improved more than controls (P < 0.004 versus P > 0.18). The difference approached significance only for the higher (10°/s; P = 0.08), but not for the slower speed tested (2°/s; P > 0.2). Controls yielded remarkably similar mean thresholds in both sessions, indicating that practice effects in this task were limited. Thus, the small improvement observed in patients might suggest some recovery in visual motion processing, but even in the second examination, patients performed significantly worse than controls in the 2°/s, but not the 10°/s, motion integration task. In summary, despite limited recovery in visual motion perception during controlled abstinence, the visual pathway for slow motion speeds remains selectively impaired in alcoholism.
Recovery of speed discrimination
In the unidirectional speed discrimination task, patients significantly improved between sessions, whereas the small reduction in thresholds of the control group did not reach significance. These results indicate some recovery beyond the practice effect in this speed discrimination task, but patients still yielded significantly higher thresholds than controls in the second session. In the second session of the bidirectional condition, controls improved thresholds, indicating a small learning effect (P = 0.14), but patients did not. The difference in thresholds between patients and controls failed to reach significance (P = 0.19), mainly due to the elevated thresholds of the controls, especially during the first examination (see above).
Recovery of divided attention
Mean RTs improved in the second session by about 50 ms, both in patients and controls, especially pronounced in the no bias (P = 0.16 and P = 0.009, in controls and patients, respectively) and global bias conditions (P < 0.0001 and P = 0.06 in controls and patients, respectively), whereas in the local bias condition, both groups had very similar RTs in both sessions (both P > 0.2). In the global bias condition, RTs decreased more in response to local than to global targets, slightly reducing the biasing effect in this condition (Fig. 7). Patients, but not controls, yielded lower error rates in all bias conditions (all P < 0.003 in patients; all P > 0.15 in controls), indicating a larger effect of practice in patients. The biasing effect was slightly reduced during the second examination in the global bias condition, since RTs of both groups decreased more for local, than for global, targets (Fig. 7
). The effect was significant in controls, but the same tendency was present in patients.
These results cannot be explained by a general decrement in RT to local, as compared to global, targets in all second examinations, since the decrease was specific for the global bias condition. Thus, whereas RTs in the no bias condition and the local bias effect were unaffected, the biasing effect in the global bias condition slightly diminished due to practice. In the first examination, patients exhibited an increased distractor effect (i.e. the difference in RTs for local targets with dissimilar versus similar global distractors was 115 ms), as compared to normal controls (84 ms). In the second session, this discrepancy disappeared, i.e. both groups yielded about the same distractor effect (81 versus 82 ms).
Recovery of visual short-term memory
In the delayed vernier discrimination task assessing visual short-term memory, both groups improved in the second, as compared to the first, examination. However, the decrease in discrimination thresholds was significant only in controls (P = 0.03), but not patients (P > 0.3). The groups did not differ significantly in visual short-term memory. This large practice effect had not been observed in a previous study applying the same task in sober and intoxicated social drinkers (Wegner and Fahle, 1999). It remains unclear why the control group in the present study significantly improved performance after training, whereas the control group of the previous study failed to do so.
In summary, the present results on the influence of chronic alcohol misuse on visual functions as assessed by psychophysical tasks indicate a deficit in visual motion processing, more specifically impairments in integrating local motion signals employed to perceive coherent motion in the presence of stimulus noise. As in acutely intoxicated social drinkers, this deficit was restricted to slow motion speeds (2°/s), arguing for a selective alcohol-related impairment in the visual stream projecting sequentially from the LGN via V1 to MT, but not the stream projecting from the LGN to both V1 and MT in parallel. Moreover, speed discrimination as assessed by random dot kinematograms remained impaired during the first 3 weeks of detoxification in patients. By contrast, visual short-term memory as tested with a delayed vernier discrimination task was not significantly deteriorated in patients as compared to matched controls. The failure to detect a significant loss in visual short-term memory was particularly due to large inter-individual differences in both groups.
To summarize the results for the visual divided attention task, both groups (recently detoxified patients and matched normal controls) demonstrated a qualitatively and quantitatively similar processing of hierarchical letters, more specifically a similar attentional capacity and capability of attentional allocation as revealed by their patterns of RTs in the bias conditions. They also showed a similar degree of practice effects. However, one exception to this correspondence between both groups was observed regarding the distractor effect, which was slightly increased in patients as compared to controls during the first session, but normal during the second examination. These results indicate that, in recently detoxified patients, the coordination of information from both hemispheres may initially be altered, resulting in an enhanced global interference on local processing. This effect seems to recover to normal levels of interference within 3 weeks of controlled abstinence. The right hemisphere hypothesis, stating that mainly right hemispheric functions are impaired in patients with chronic alcohol misuse, would predict: (a) faster RTs to local target levels (processed in the left hemisphere) than to global levels (processed in the right hemisphere); (b) a reduction in interference of global information (right hemisphere) with local processing (left hemisphere). The present pattern of results, i.e. no preference in RTs for a certain target level together with the enlarged distractor effect, contradicts the predictions of the right hemisphere theory of alcoholism.
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ACKNOWLEDGEMENTS |
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FOOTNOTES |
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