scale of the attentional focus and the effect of aging and DAT on those changes. Pamela M. Greenwood and Raja Parasuraman, Cognitive Sci- ence Laboratory ...
Neuropsychology 1997, Vol. 11, No. 1,3-12
Copyright 1997 by the American Psychological Association, Inc. 0894-4105/97f$3.00
Controlling the Focus of Spatial Attention During Visual Search: Effects of Advanced Aging and Alzheimer Disease Pamela M. Greenwood and Raja Parasuraman The Catholic University of America
Gene E. Alexander National Institute on Aging
It was hypothesized that slowed visual search in healthy adult aging arises from reduced ability to adjust the size of the attentional focus. A novel, cued-visual search task manipulated the scale of spatial attention in a complex field in healthy elderly individuals and patients with dementia of the Alzheimer type (DAT). Precues indicated with varying validity the size and location of the area to be searched. Location precues exerted the strongest effects on conjunction search and the weakest effects on feature search. As the size of valid location cues decreased, conjunction search was facilitated. These effects declined progressively with advanced age and the onset of DAT. As the size of invalid cues increased, conjunction search was first facilitated, then slowed, but neither age nor DAT altered this effect. These results indicate that both Alzheimer's disease and, to a lesser degree, advanced aging, reduce control of the spatial focus of attention.
Older adults diagnosed with dementia of the Alzheimer type (DAT) exhibit a variety of attentional impairments in addition to their memory deficits. A recent review concluded that the shifting of selective visual attention and divided attention are prominently affected in the mild, early stages of Alzheimer disease (Parasuraman & Haxby, 1993). One aspect of selective visual attention, termed visuospatial or covert visual attention, is the ability to attend selectively to a particular region of extrapersonal space so that information at that location is obtained with increased speed and accuracy (e.g., Hawkins et al., 1990). Based on work with the location precue paradigm, Posner and colleagues (Posner, Walker, Friderich, & Rafal, 1984) have postulated separate componential processes of visuospatial attention: engaging, shifting, and disengaging. In response to a location cue, attention is engaged at the cued location. If the cue is invalid, attention must be disengaged from this cued location, and then shifted to the target location. Based on work with the visual search paradigm, Treisman and Gelade (1980) postulated that serial shifts of visuospatial attention are essential for search for conjunctions of features in large stimulus arrays. The present study looks beyond shifts of visuospatial attention to the issue of dynamic changes in the scale of the attentional focus and the effect of aging and DAT on those changes.
Pamela M. Greenwood and Raja Parasuraman, Cognitive Science Laboratory, The Catholic University of America; Gene E. Alexander, Laboratory of Neurosciences, National Institute on Aging, Bethesda, Maryland. This research was supported by an Alzheimer's Association/Ana M. Buchanan Memorial Investigator-Initiated Research Grant and Research Grants AG123987 and AG07569 from the National Institute on Aging. Correspondence concerning this article should be addressed to Pamela M. Greenwood, Cognitive Science Laboratory, Psychology Department, The Catholic University of America, Washington, DC 20064.
Parasuraman, Greenwood, Haxby, and Grady (1992) showed that compared with healthy age-matched controls, individuals with DAT were selectively deficient in spatial shifting of visual attention, specifically in the disengagement of attention from an incorrectly cued location (Posner et al., 1984). This finding has been replicated in subsequent studies in which measures of both covert (Maruff, Malone, & Currie, 1995; Oken, Kishiyama, Kaye, & Howieson, 1994) and overt attention (eye movements; Scinto et al., 1994) were used. In addition, persons with DAT also exhibit impairments in shifting attention: (a) between different features (Haxby, Parasuraman, Gillette, & Raffaele, 1991) or levels of organization of a composite visual object (Filoteo et al., 1992; Massman et al., 1993), (b) between visual and auditory modalities (Berardi, 1994), and (c) from one stimulus "set" or categorization rule to another (Grady et al., 1988; Sahakian, Sownes, & Eagger, 1990). These findings suggest that the attention-shifting deficit in DAT is pervasive. Nevertheless, the impairment is selective in terms of the underlying components affected for both persons with DAT and healthy older adults. First, neither age nor DAT alter the characteristics of visuospatial attention when only a simple detection task must be performed at the attended location (e.g., luminance onset or the appearance of a single letter; Greenwood, Parasuraman, & Haxby, 1993; Greenwood & Parasuraman, 1994; Hartley, Kieley, & Slabach, 1990; Nissen & Corkin, 1985; Parasuraman et al., 1992; Robinson & Kertzman, 1990). Second, even when attention must be shifted to a location in order to perform a more demanding discrimination task (e.g., letter discrimination), the ability to engage the target in response to a valid location cue remains unaffected either by aging (Greenwood & Parasuraman, 1994) or by DAT (Parasuraman et al., 1992). It is only when invalid location cues are given that the ability to redirect attention is impaired in both cases. There is modest slowing of the disengagement of attention up to about age 75 in healthy nondemented adults (Greenwood et
GREENWOOD, PARASURAMAN, AND ALEXANDER al., 1993; Hartley et al., 1990). This effect increases progressively with age, so that "old-old" nondemented elderly persons (aged 75 to 85) are slowed more on invalid-cue trials than are "young-old" adults aged under 75 (Greenwood & Parasuraman, 1994). The disengagement deficit is even more marked in DAT patients (Parasuraman et al., 1992). These results can be summarized by stating that when attention must be shifted to a location in order to discriminate a target, neither advanced age (over 75) nor DAT affect the ability to engage the target given a correct location cue. However, both conditions impair the disengagement of attention from an invalidly cued spatial location. One limitation of these studies is that they examined attention shifting in relatively impoverished visual environments. Typically, participants were required to engage or disengage attention to targets presented in an otherwise empty visual field. A better simulation of everyday vision is a task in which the target appears along with abstractors in the visual field. Any difficulty in redirecting or disengaging visuospatial attention should become more evident if repeated shifts of attention are required to search for a target surrounded by distractors. If so_search tasks should be more sensitive to slowed disengagement than nonsearch tasks. Moreover, such a task would also provide a more rigorous test of the hypothesis that engagement is unaffected by age or DAT. Treisman and Gelade (1980) have theorized that search for a target defined by a conjunction of elementary features (such as color, orientation, motion, etc.) requires serial examination of each item and thus the repeated deployment of visuospatial attention across the visual field. Thus, search time increases with the number of distractors in the display. In contrast, search for targets that differ from distractors by a single, salient feature—producing the phenomenon of "pop-out"—is thought to proceed hi parallel, without the need for shifts of visuospatial attention. Recent work has questioned whether these two types of search are fundamentally and qualitatively different (Duncan & Humphreys, 1989; Nakayama & Silverman, 1986). Duncan and Humphreys (1989), for example, have suggested that feature and conjunction search represent two extremes along a continuum of search difficulty defined by target-distractor and distractor-distractor similarity. Nevertheless, there is agreement that when targets and distractors are easily discriminable, visual search can occur quickly without regard for the number of distractors and without shifts of attention, whereas when targets and distractors are less discriminable, search time increases linearly with the number of distractors (the "search function"). The positive slope of the search function for difficult or conjunction targets is probably due to a mechanism involving serial shifts of visuospatial attention. Healthy adult aging differentially affects feature and conjunction search. Plude and Doussard-Roosevelt (1989) found that search for easily discriminable feature targets was minimally affected by age, whereas the search function for conjunction targets was slowed (i.e., had a larger slope) in older relative to younger adults. In contrast. Oken, Kishi-
yama, and Kaye (1994) did not find steeper RT search slopes in two groups of elderly persons (aged 60 to 99), although they did find steeper accuracy search slopes. Possibly the limited display durations of 800 and 1,800 ms may have obscured an RT/age function in the elderly participants by eliminating long RTs. Consistent with the views of Triesman (e.g., Treisman & Gelade, 1980) and of Posner (Posner & Dehaene, 1994), age-related slowing of the conjunction search function may be attributable to an underlying deficiency in the processes involved in successively engaging and disengaging visuospatial attention from one item to the next. We hypothesize that this age-related slowing in attentional shifting arises from a reduction in the ability to adjust the size of the focus of spatial attention. Studies with healthy young adults indicate that the effective area or scale of the attentional focus can be voluntarily adjusted, as if spatial attention operated like a zoom lens (Castiello & Umilta, 1990; Eriksen & Yeh, 1985). In covert-attention tasks with central cues, a relatively large (and generally empty) area such as an entire visual hemifield is primed. Participants are required to detect or identify a target presented somewhere in that field or in the opposite hemifield. If the target is smaller than the cued area, as is often the case, then older adults might be slower to redirect attention on invalid trials if they were less able to change the focus of spatial attention from the large scale of a visual hemifield to the smaller scale of the target. Although any such deficiency may not be important when the task is easy (hence the lack of effects of age or DAT in detection tasks), it may be a salient factor when harder discriminations are required at the attended location. It may be a particularly salient factor in conjunction search when a small target must be discriminated from surrounding distractors. We tested this hypothesis by manipulating the focus of spatial attention during visual search by young-old, old-old, and DAT participants. A novel, cued-visual search task was developed. Location precues differing in spatial precision (size and location) and validity were used to control the need for redirection of the location and adjustment of the scale of spatial attention. Varying precue location allows questions about the effect of aging and DAT on the ability to engage and disengage visuospatial attention. Varying the difficulty of search by manipulating the discriminability of targets and distractors evaluates whether age and DAT differentially alter the scale of the attentional focus in easy and in hard search. Manipulating precue size allows questions about the effect of age and DAT on the ability to flexibly adjust the scale of the attentional focus. Previously, we have shown that both nondemented old-old participants and participants with mild DAT are slower to make large movements of attention away from the invalidly cued visual field (Greenwood & Parasuraman, 1994; Parasuraman et al., 1992). We therefore predicted that the ability to make small shifts of attention within a visual field will also be progressively impaired by advanced age and DAT in harder conjunction search but not in easier feature search.
SPATIAL ATTENTION DURING VISUAL SEARCH
Method Participants The DAT group was composed of 12 individuals in the early stage of DAT meeting the National Institute for Neurology, Communicative Disorders, and Stroke—Alzheimer's Disease and Related Disorders Association (NINCDS-ADRDA; McKhann et al., 1984) diagnostic criteria for probable Alzheimer's disease and 2 otherwise healthy adults meeting the criteria for possible Alzheimer's disease. All 14 individuals with DAT (ages 50-84) were participants in an ongoing longitudinal study at the Laboratory of Neurosciences of the National Institute on Aging. Full details of the clinical and neuropsychological testing procedures can be found elsewhere (Haxby et al., 1986). The young-old (ages 63-74) and old-old (ages 75-81) groups were each composed of 14 volunteers screened for health status on the basis of a questionnaire. By self-report, none were using medications that could adversely affect attentional functions (Giambra & Quilter, 1988). Old participants were recruited by newspaper advertisement and paid for their participation. The young-old group was matched in age to the DAT group. Gender and means of age, years of education, Mini-Mental state (Folstein, Folstein, & McHugh, 1975), and score on the Logical Memory subtest of the Wechsler Memory Scale (Russell, 1975; Wechsler, 1945) for each group are shown in Table 1. The DAT group differed significantly from the two healthy elderly groups on years of education, F(2, 39) = 4.64, p < .02. All groups differed significantly from each other in performance on both immediate and delayed Logical Memory subtests, p < .05. Because we have previously reported mean Logical Memory scores that are similar to those of the present old-old group (10.9 for young participants, 11.3 for young-old participants, and 11.6 for old-old participants; Greenwood & Parasuraman, 1994), the significant difference between young-old and old-old groups can be attributed more to high scores of the young-old than to low scores of the old-old. Cued-Visual Search Task A cued-visual search task was developed to allow cuing with variable precision of the location of a target letter in an array of letters in the form o f a 2 X 5 o r 3 X 5 matrix. Following a fixation point ( I s duration), a rectangle appeared for 500 ms before the array of letters was presented. The rectangle was the location cue. Cue size varied from a rectangle that surrounded one letter (high precision of localization), to one column of letters (medium precision), to the entire array of letters (low precision). The letter Table 1 Croup Means and Standard Deviations for Subject Characteristics
array consisted of 10 (7.4 X 2.9°) or 15 (7.4 X 4.8°) upper-case characters (i.e., display size was either 10 or 15). The characters were three letters (T, N, G) drawn in one of three colors (green, blue, or pink). The order and position of the letters comprising the array were chosen randomly. The inner edge of each array appeared to the right or left of fixation by 3.8° and remained on the screen either until the participant responded or 2 s elapsed. In all conditions, the same target, a pink T, appeared in the array on half the trials and was absent on the other half of the trials. Participants were required to respond on each trial to the presence or absence of a pink T by pressing one of two buttons with the index fingers.
Cue Conditions Cues were valid on 80% and invalid on 20% of the trials. Targets were either present or absent, but cues could not be valid when the target was absent. As noted previously, cues to target location were rectangles surrounding one letter (area = 2 cm2, 1.7° X 1.4°), one column of letters (mean area = 5.2 cm2, 1.3° X 3.6° for 10 letters and 1.3° X 5.5° for 15 letters), or an entire array of letters (area = 37.6 cm2, 7.2° X 5.5°). For the two smaller cue sizes, invalid cues indicated locations within the array that did not include the target. For the largest cue size, an invalid cue was centered in the half of the screen opposite to that in which the target would appear.
Search Conditions Tasks were designed to elicit three types of search, the standard feature and conjunction search tasks, and a third "combined" search task. Subjects were required to search for the same target, a pink T, in all three conditions: (a) search for a single feature, termed color search, in which only one item in the display was the target color (pink); (b) search for a conjunction of target color (pink) and letter form (T), termed color + letter search, in which the target properties of color and form appeared with equal frequency; and (c) combined search, where the number of target color (pink) distractors was restricted to two, the remainder being blue and green. It has been shown that young adults are able to confine conjunction search to those items sharing a salient property (color, form) with the target (Egeth, Vizri, & Garbart, 1984), presumably by first selecting as a whole those items possessing the shared property and subsequently searching for the target only through those selected items. Plude and Doussard-Roosevelt (1989) observed that this ability remains intact in older adults. This combined search condition was included in the present study so that we could examine whether this ability becomes compromised by advanced age, or by the onset of DAT, or both.
Group Characteristic
Young-old
Old-old
DAT
Age Education Gender (F, M) Logical memory (WMS) Immediate Delayed Mini-Mental State Exam
67.9 (3.6) 16.9 (2.2) 10,4
77.5(1.6) 16.2 (2.9) 5,9
70.6(9.5) 13.9(3.1) 10,4
15.9 (2.8) 15.0(2.5)
11.9(3.2) 11.1 (3.2) 28.9(1.2)
3.4 (2.4) 0.9(1.8) 23.9 (3.9)
Note. Standard deviations are in parentheses. DAT = dementia of the Alzheimer type; F = female; M = male; WMS = Wechsler Memory Scale.
Procedure 'Bask conditions were mixed within the total of 1,380 trials. Trials were presented hi six counterbalanced blocks of 230 randomly ordered trials. Each trial began with a centered warning plus sign presented for 500 ms, which was followed by the cue. After a 500ms cue-target stimulus onset asychrony (SOA), the array of letters appeared superimposed over the cue. Both cue and array remained present either until the participant responded to the presence or absence of the target or until 2.5 s elapsed. A 10-min rest was given after the first three blocks.
GREENWOOD, PARASURAMAN, AND ALEXANDER
Data Analyses After eliminating reaction times (RT) of less than 100 ms, accuracy scores and median RTs for correct responses were computed for each condition. The RT data were submitted to mixed-factorial analyses of variance (ANOVA). Factors were group (young-old, old-old, DAT), search condition (color, color + letter, combined), presence or absence of target (PA), cue validity (valid, invalid), display size (10, 15), and cue size (small, medium, large), but the cue validity and PA factors were not completely crossed. Repeated measures F values were corrected for violations from sphericity (Keselman & Rogan, 1980) by adjusting degrees of freedom (Huynh & Feldt, 1970). Post hoc contrasts of group effects used the Student-Newman-Keuls post hoc test (Winer, Brown, & Michels, 1991). Because the design of this experiment was not completely crossed (i.e., there could not be valid-cue trials on which the target was absent), analysis of cue validity effects could only be performed for target-present trials, and analysis of the effects of target presence or absence could only be done for invalid-cue trials.
Results Accuracy There were no significant effects involving group on accuracy of target identification for any of the three search conditions (color, color + letter, and combined). For color search, accuracy ranged from 93.8% to 98.9%. For the more difficult color + letter condition, accuracy ranged from 78.6% for the old-old group following an invalid cue of the largest size to 97.9% for the young-old group following a middle-sized valid cue. For combined search, the range was 89.3% to 97.5%.
rately. In addition, significant cue-validity effects were obtained in each of the ANOVAs carried out for the separate search task conditions. Hence, analyses were further separated for valid-cue and invalid-cue trials. Several interactions were also significant in the omnibus ANOVAs, but these are further elucidated in the separate-task ANOVAs.
Color Search Valid-cue trials. Mean RTs for the valid-cue trials are plotted as a function of cue size in Figure 1. The RT/cue-size functions were relatively flat. RTs increased with advanced age and DAT, F(2, 39) = 8.84, p < .001, and with display size, F(l, 39) = 17.96, p < .0001. Although there was an interaction of Display Size X Cue Size, F(2,78) = 5.81,p < .01, RTs did not vary significantly between groups as a function of display size or cue size. Treisman's (1985) view that feature search proceeds in parallel and independently of the number of display items predicts that precues should also have little effect on feature search RTs. If so, the regression of RT on cue size should yield a zero slope. In fact, the mean slopes (milliseconds per square centimeter of cue size) were close to zero and did not differ significantly between the groups (.720, .444, and -.135 for the young-old, old-old, and DAT groups, respectively). The ANOVA of the slope values showed a significant main effect of display size only, F(l, 39) = 11.52,p < .002, which Figure 1 shows was due to slowed RT with the 15-item array and the largest cue. However, the absence of group effects indicates that this phenomenon was unaffected by aging or DAT. Thus, single-feature (color) search produced target pop-
COLOR SEARCH - VALID TRIALS
Reaction Time In order to assess the presence of differential fatigue effects of the groups, simple reaction time (SRT) was recorded before and after the task blocks. This data was complete only for the DAT and old-old groups. Although an ANOVA indicated that the participants with DAT were slower overall (p < .03), the difference between pretask SRT (M = 369.1 ms) and posttask SRT (M = 375.0 ms) was not significant, nor was there an interaction with group. Therefore, any fatigue effects were very small and were not differential for the DAT and old-old groups. Omnibus ANOVAs were performed on the invalid-cue and target-present trials separately. Because the number of significant effects was large, results of the omnibus analyses are only summarized here and additional analyses are reported fully later. For the invalid-cue ANOVA (group, search condition, target presence or absence, cue size and display size), all main effects except group were significant (p < .01). For the target-present ANOVA (group, search condition, cue validity, cue size and display size), all main effects except search condition were significant (p < .05). There was also a significant three-way interaction between search condition, display size, and cue size (p < .02). The significant effects involving search condition in each of these analyses justified analyses of each search task sepa-
Young old -DS10 OldOld-DSIO DAT-DS10 YoungOld-DS15 CMOIU-OS15 DAT-DS15
CUE SIZE (cm2)
Figure 1. Reaction time (RT) as a function of valid cue size in the color search task for the three groups at two display sizes (DS10 andDS15). DAT = dementia of the Alzheimer type.
SPATIAL ATTENTION DURING VISUAL SEARCH
out in participants with DAT and in both older groups that was largely unaffected by experimental manipulations except when a large array-sized area was cued. Invalid-cue trials. RT was slowed when the target was absent, PA, F(l, 39) = 6.71, p < .01, particularly in the old-old group, Group X PA, F (2, 39) = 6.81, p < .003. RT was also slowed by advanced age and DAT, F(2, 39) = 5.73, p < .01, and by increases in display size, F(l, 39) = 27.65, p < .0001, and cue size, F(2, 78) = 188.42, p < .0001. The Cue Size X Group, F(4, 78) = 5.20, p < .005, and Cue Size X PA, F(2, 78) = 50.24, p < .0001, interactions were also significant. Figure 2 shows that the RT/cue size function was not linear for invalid-cue trials. RT first decreased and then increased as cue size increased. Calculation of the simple effects of group at each cue size showed that RTs differed significantly between groups at the two smaller cues (p < .05), but not at the larger cue. Figure 2 also shows that cue size effects decreased progressively in the old-old and DAT groups compared with the young-old group. The slowing of RT when the cue is large and invalid may reflect the slowing effect of a large focus of attention, seen in Figure 1, combined with the need to shift attention from one visual hemifield to the other, necessary only for the large cue. Based on our previous findings of increased slowing on invalidly cued trials in advanced age and DAT (Greenwood & Parasuraman, 1994; Parasuraman et al., 1992), it could be predicted that the increase from the middle-sized to the
largest cue would be greater for the old-old and DAT groups. To test this prediction, the difference between the largest and middle-sized cue was calculated. There were significant differences between groups, F(2, 39) = 5.10, p < .01, but opposite to that predicted: 195.9 ms, 160.5 ms, and 117.3 ms for the young-old, old-old, and DAT groups, respectively. Figure 2 also shows that RTs were also somewhat slowed on invalid trials following the smallest compared with the middle-sized cue, again when display size was large. A separate analysis of the two smaller cue sizes showed that RT was slower following the smallest cue (M - 625.9 ms) compared with the middle-sized cue (M = 599.6 ms) but only when the array size was large, Display Size X Cue Size interaction, F(l, 39) = 7.74, p < .001. There were also significant main effects of group, F(2, 39) = 4.70, p < .02, and display size, F(l, 39) = 5.77, p < .02.
Color Plus Letter Search Valid-cue trials. Mean RTs for die valid-cue trials, averaged over display sizes, are plotted as a function of cue size in Figure 3. RTs increased monotonically with cue size. Search was fastest for the letter-size cue, intermediate for the column-size cue, and slowest for the array cue. RTs increased with age and DAT, F(2, 39) = 10.68, p < .0002, display size, F(l, 39) = 122.59, p < .0001, and cue size, F(2,78) = 21.51, p < .0001. Effects of cue size were greater at the larger display size, F(2, 78) = 5.64, p
