Age-related dedifferentiation of visuospatial abilities

Transcription

1 Neuropsychologia 40 (2002) Age-related dedifferentiation of visuospatial abilities Jing Chen a,, Joel Myerson b, Sandra Hale b a Department of Psychology, Grand Valley State University, Allendale, MI 49401, USA b Department of Psychology, Washington University, St. Louis, MO, USA Received 28 June 2001; received in revised form 3 April 2002; accepted 3 April 2002 Abstract Forty-eight older adults were tested on a battery of seven speeded visuospatial tasks that were developed by Chen et al. [4] to measure the functions of the ventral and dorsal neural processing streams. Principal components analysis revealed only one factor with an eigenvalue greater than 1.0, and all of the tasks loaded heavily on this general factor. These results are in contrast to those reported in a previous study of young adults in which principal components analysis revealed two factors with eigenvalues greater than 1.0 [4]. Importantly, for young adults the second principal component was a bipolar factor which grouped the tasks based on the neural processing stream (i.e. ventral versus dorsal) whose function they had been designed to assess. The age-related difference in the factor structure of visuospatial abilities apparent from the present results may be interpreted as reflecting an age-related dedifferentiation of the neural processing streams consistent with the results of recent neuroimaging studies [12,13] Elsevier Science Ltd. All rights reserved. Keywords: Aging; Visuospatial abilities; Ventral stream; Dorsal stream 1. Age-related dedifferentiation of visuospatial abilities Studies using neuropsychological and neuroimaging techniques provide converging evidence that information about the visual features of objects and information about their spatial locations are processed by separate neural systems [13,15,17,25]. These specialized neural systems have been termed the ventral processing stream and the dorsal stream, and they deal primarily with object feature and location information, respectively [34,24]. Nevertheless, there are extensive neuroanatomical connections between the two streams [10]. This has lead some researchers to stress the interactive nature of information processing in the visual system as a whole and to de-emphasize the specialized functions of components like the dorsal and ventral streams [22,35]. In a recent behavioral study, Chen et al. [4] examined whether, despite the extensive interconnections between the two streams, they are sufficiently functionally independent to be reflected in individual differences in visuospatial abilities. In order to examine the relationship between the structure of visuospatial abilities and the organization of the underlying visual system, Chen et al. used a battery of seven speeded tasks that were designed based on neurobiological studies of ventral and dorsal stream functions: three tasks Corresponding author. Tel.: ; fax: address: chenj@gvsu.edu (J. Chen). were constructed to assess primarily ventral functions [7,8,29,30,32,33] and four were constructed to assess primarily dorsal functions [1,9,15,20,21,23,26]. More specifically, the putative ventral tasks involved comparing irregular shapes regardless of differences in size, color, or contrast and integrating object feature information, such as shape, color, and texture; the putative dorsal tasks involved making judgments about object locations, shifting spatial attention, and mentally rotating objects in two-dimensional and three-dimensional space. Chen et al. [4] used principal components analysis to examine the structure of visual abilities in young adults. There were only two factors with eigenvalues greater than 1.0. The first principal component represented a general factor. Importantly, the second principal component grouped the tasks according to the neural processing stream (ventral versus dorsal) whose function a particular task had been designed to assess. Specifically, the second principal component was a bipolar factor on which the ventral tasks loaded positively and the dorsal tasks loaded negatively [4]. These results are consistent with the hypothesis that individual differences in visuospatial abilities reflect individual differences in the efficiency with which the two streams process information, at least in young adults. However, neuroimaging studies provide reason to question whether findings with young adults generalize to older adults (for a review, see [14]). For example, activation patterns for face discrimination and location matching tasks show a clear dissociation of the dorsal and /02/$ see front matter 2002 Elsevier Science Ltd. All rights reserved. PII: S (02)00060-X

2 J. Chen et al. / Neuropsychologia 40 (2002) ventral streams in young adults [15] whereas in older adults, this dissociation is less complete [13]. In addition, older adults show greater frontal activation than young adults on a variety of tasks, and Grady [14] has suggested that this may help older adults to compensate for losses in efficiency in other aspects of brain function. In short, neuroimaging data suggest that normal aging is accompanied by a dedifferentiation of the activation patterns of the ventral and dorsal streams [12]. The purpose of the current study was to determine whether the observed dedifferentiation in neural activation is associated with a dedifferentiation that can be identified behaviorally. Such behavioral dedifferentiation is predicted by the hypothesis that the structure of visuospatial abilities reflects individual differences in the efficiency with which the two streams process information. Accordingly, a group of older adults were tested on the battery of visuospatial perceptual tasks developed by Chen et al. [4] in order to determine whether the same factor structure of visuospatial abilities observed in young adults would also be observed in an older adult group Unnameable shapes or not two irregular polygons shared the same shape regardless of their differences in color and size. Two conditions were included in this task (see sample stimuli in panel 1 of Fig. 1): same shapes condition and different shapes condition. 2. Methods 2.1. Subjects Forty-eight healthy older adults from the pool of volunteers maintained by the Department of Psychology at Washington University were tested. All of the participants had normal or corrected to normal vision. The age range was years, and the average age for the group was 70.9 years (S.D. = 2.4) Apparatus Stimuli were presented on a NEC MultiSynch 2A monitor controlled by a CompuAdd 286 IBM-compatible computer. The software to control the experiment (developed by the third author, S.H.) used routines from the PCX Toolkit (Genus) to synchronize stimulus presentation with the video refresh cycle, thereby permitting response times (RTs) to be measured with 1 ms accuracy. The response panel contained three buttons arranged in an inverted triangle. The two upper (right and left) buttons were used to report decisions, and the lower center button was used to initiate trials Tasks A battery of seven visuospatial tasks was administered to participants. Three tasks (i.e. unnameable shapes, puzzle pieces, and abstract matching) were used to assess the ventral functions and four tasks (i.e. dot location, curve tracing, two-dimensional mental rotation and three-dimensional mental rotation) were used to assess the dorsal functions. The following is a brief description of the tasks (for more details, see [4]). Fig. 1. Sample stimuli from the seven tasks. Panel 1 (top). Unnameable shapes (left: same shapes; right: different shapes). Panel 2. Puzzle pieces (from left to right: two-protrusions, same; two-protrusions, different; four-protrusions, same; four-protrusions, different). Panel 3. Abstract matching (left: level one; middle: level two; right: level three). Panel 4. Dot location (left: shorter distances; right: longer distances). Panel 5. Curve tracing (left: short distance; right: long distance). Panel 6. Two-dimensional mental rotation (left: 72 rotation; right: 144 rotation). Panel 7. Three-dimensional mental rotation (left: same arrangement; middle: different-untransposed; right: different-transposed). The upper three panels represent the tasks hypothesized to depend on ventral stream functions, and the lower four panels represent the tasks hypothesized to depend on dorsal stream functions.

3 2052 J. Chen et al. / Neuropsychologia 40 (2002) Puzzle pieces a puzzle piece would fit into the space in the center of an incomplete puzzle. The puzzle piece and the space in the puzzle both had either two-protrusions or four-protrusions. The puzzle piece never had to be turned to fit into the puzzle. Four conditions were included in this task (see sample stimuli in panel 2 of Fig. 1): (1) two-protrusions, same shapes; (2) two-protrusions, different shapes; (3) four-protrusions, same shapes and (4) four-protrusions, different shapes Abstract matching In this task, participants were required to decide which of the two top objects was a better match to the object at the bottom. The objects could be matched on three dimensions: shape, color, and texture. Three conditions were included (see sample stimuli in panel 3 of Fig. 1): (1) level one one of the upper objects was identical to the bottom object; (2) level two one of the upper objects matched to the bottom object on two dimensions, and the other object matched to the bottom object on only one dimension; (3) level three one of the upper objects matched the bottom object on one dimension, and the other object differed from the bottom object on all three dimensions Dot location a white dot on the left or a white dot on the right was closer to a center red dot. Two conditions were included in this task (see sample stimuli in panel 4 of Fig. 1): a shorter distances condition and a longer distances condition Curve tracing or not two red dots were both on the same curved line. To do this, they were instructed to look at the red dot on the left first, and then follow the curved line it was on until they reached a second dot. Two conditions were included in this task (see sample stimuli in panel 5 of Fig. 1): a short distance condition and a long distance condition Two-dimensional mental rotation the dot in the right pentagon had the same location as the dot in the left pentagon after the right pentagon was mentally rotated until its double line was also at the bottom. Two conditions were included (see sample stimuli in panel 6ofFig. 1):a72 rotation condition and a 144 rotation condition Three-dimensional mental rotation the two buildings in the top view (i.e. the left display) were in the same locations as the two buildings in the side view (i.e. the right display). Three conditions were included in this task (see samples in panel 7 of Fig. 1): (1) same arrangement; (2) different arrangement (untransposed) the distance between the two buildings in the left display was different from that in the right display and (3) different arrangement (transposed) in addition to the difference in distance, the building on the right in the top view appeared on the left in the side view, and vice versa Procedure The tasks were presented in the following order: unnameable shapes, curve tracing, puzzle pieces, dot location, three-dimensional mental rotation, abstract matching, and two-dimensional mental rotation. This order was used to alternate tasks from different streams as well as to prevent the covariation of task difficulty with practice or fatigue. Each participant performed the tasks in the same order. To initiate each trial, participants were instructed to press the lower button on the response panel. Each trial began with the presentation of a fixation point. Following a 200 ms delay, the stimulus was presented and would remain on the screen until the participant pressed one of the two upper buttons or until a 10 s period lapsed. Feedback (a computer beep) was given if an error was made or no response was made within 10 s. After a correct response or a computer beep, the screen remained blank for 700 ms, and then the fixation point for the next trial was presented. Prior to the presentation of experimental trials for each task, there were six practice trials and two buffer trials that were not included in any of the analysis. 3. Results Table 1 presents older adults mean RTs, standard deviations, and error rates for each task condition. For comparison, the corresponding data for young adults tested using the same apparatus and procedure, previously reported by Chen et al. [4], are also presented. Averaged across tasks, the age difference in error rates was less than 0.5% (young M = 3.89%; old M = 4.35%). Thus, although older adults were, on average, slower than young adults in every condition, it is unlikely that such slowing was due to an age difference in speed-accuracy trade-off. Correlations between older adults RTs are presented in Table 2, along with the corresponding young adult correlations from Chen et al. [4]. For young adults, the correlations between tasks that tapped the functions of the same stream (given in bold italics) were much stronger than the correlations between tasks that tapped functions of different

4 J. Chen et al. / Neuropsychologia 40 (2002) Table 1 Mean RTs (ms), standard deviations (S.D.), and error rates (%) for older adults and young adults on seven tasks Task Mean RT S.D. Error (%) Old Young Old Young Old Young Unnameable shapes Same Different Puzzle pieces Two-protrusions, same Two-protrusions, different Four-protrusions, same Four-protrusions, different Abstract matching Level one Level two Level three Dot location Shorter distances Longer distances Curve tracing Short distance Long distance Two-dimensional mental rotation 72 rotation rotation Three-dimensional mental rotation Same arrangement Different (untransposed) Different (transposed) Data on young adults are from Chen et al. [4]. streams. More specifically, the mean correlation between tasks from different streams was only 0.381, whereas the mean correlation between ventral tasks was and the mean correlation between dorsal tasks was (A Fisher Z transformation was performed on all correlations before averaging.) For older adults, in contrast, the mean correlation between different stream tasks was 0.467, whereas the mean correlation between ventral tasks was and the mean correlation between dorsal tasks was Thus, for older adults the correlations between tasks that tapped the function of two different streams were similar in strength to the correlation between tasks that tapped functions of the same stream. The mean correlation results reflect the fact that when the corresponding task correlations of young and older adults are compared one by one, most (eight out of nine) of the within-stream correlations for the young adults are larger than those for the older adults, whereas most (8 out of 12) of the between-stream correlations for the older adults are larger than those for the young adults (see Table 2). Interestingly, older adults failed to show the young adult pattern of stronger covariation between RTs on tasks that assessed Table 2 Correlation matrix of the RTs between seven visual spatial tasks Tasks Unnameable shapes Puzzle pieces Abstract matching Dot location Curve tracing Two-dimensional mental rotation Three-dimensional mental rotation Note: correlations for older adults are above the diagonal and those for young adults [4] are below the diagonal. Correlations between tasks from the same stream are in bold italics.

5 2054 J. Chen et al. / Neuropsychologia 40 (2002) Table 3 Factor loadings from principal components analysis of older and young adults reaction times (results for young adults from Chen et al. [4]) Tasks Principal components Component 1 Component 2 Old Young Old Young Unnameable shapes Puzzle pieces Abstract matching Dot location Curve tracing Two-dimensional mental rotation Three-dimensional mental rotation functions of the same stream despite the fact that the degree of covariation overall was comparable for the two groups. The mean r for young adults was 0.499, whereas the mean r for older adults was Table 3 presents the results of a principal components analysis conducted on older adults RTs as well as the results of a principal components analysis of young adults RTs on the same tasks reported by Chen et al. [4]. Although analysis of the young adults RTs revealed two principal components with eigenvalues greater than 1.0 [4], the analysis of older adults RTs revealed only one principal component with an eigenvalue greater than 1.0. All tasks loaded heavily on this component (eigenvalue = 3.80) that accounted for approximately 54% of the total variance in data space, and the factor loading was similar to that for the first principal component for young adults [4]. In young adults, the pattern of loadings on the second principal component was consistent with the division of the tasks into those tapping ventral stream functions and those tapping dorsal stream functions (with the former loading positively and the latter loading negatively), whereas in the older adults, no such correspondence was observed. 4. Discussion The present results reveal a picture of the factor structure of older adults visuospatial abilities that differs from that which is seen with young adults. Compared with the older adults, young adults showed much stronger correlations between tasks from the same stream and weaker correlations between tasks from different streams. Principal components analysis provides a way of summarizing intercorrelation patterns, and in the present case, the critical difference between the two age groups lies in the second principal component. In young adults, the second principal component grouped the tasks according to the neural processing stream (ventral versus dorsal) whose function a particular task had been designed to assess [4]. However, the second component was much weaker in older adults, suggesting that the differentiation in visuospatial abilities identified in young adults begins to break down in older adults. Taken together with the results of neuroimaging studies which suggest that the functional distinction between the ventral and the dorsal streams is decreased in older adults [12], the dedifferentiation in older adults visuospatial abilities observed in the current study suggests that the functional organization of the brain s visual system may be directly reflected in the behavioral structure of visuospatial abilities. It should be pointed out that even though the differentiation between ventral and dorsal functions was weaker in older adults, they did show some behavioral evidence of the pattern of brain-based visuospatial abilities observed in young adults. For example, although the second principal component was below the conventional cutoff level (eigenvalue < 1.0), it did account for an additional 14% of the variance in the older adult data (compared with the 20% value for the young adult data). Additionally, although some caution needs to be taken in interpreting this component because of its low eigenvalue, the factor loading pattern for older adults is somewhat consistent with the underlying neural categories. More specifically, two out of three ventral tasks loaded positively and three out of four dorsal tasks loaded negatively on this component. These results parallel the findings from neuroimaging studies [12] in that the functional distinction between the ventral and dorsal streams appeared to be present in older adults, although it was clearly much weaker than in young adults. One task whose intercorrelations appear to have contributed to the dedifferentiation pattern is abstract matching. This task, which consists of making multi-dimensional similarity judgments (see Fig. 1), may involve abstract reasoning as well as visuospatial information processing, and it also may be especially susceptible to the use of alternative strategies. For example, the fact that the correlation between abstract matching and curve tracing is approximately twice as strong in older adults as it is in young adults raises the possibility that older adults use a serial strategy involving more attention shifting. That is, perhaps older adults were comparing objects on one dimension at a time whereas young adults may have been capable of simultaneous comparisons. This hypothesis of an age-related strategy shift is, of course, purely speculative and would require further testing.

6 J. Chen et al. / Neuropsychologia 40 (2002) The trend toward dedifferentiation with age is not unique to the visuospatial functions measured in the present study. Psychometric studies comparing young and older adults have frequently reported evidence of age-related dedifferentiation of cognitive abilities. Based on fluid/crystallized intelligence measures, for example, Baltes et al. [3] reported that the number of mental ability factors was smaller for older adults than for young adults. Other studies have reported that the covariation among specifically speed-related abilities [2] was greater for older adults than for young adults, and similar results have been reported for cognitive abilities measured by various psychometric batteries [6,16,31]. A growing number of neuroimaging studies have reported that when performing cognitive tasks, older adults activated additional brain areas beyond the ones activated in young adults, and this phenomenon may underlie the dedifferentiation observed behaviorally [18]. Notably, the tasks used in these neuroimaging studies have been diverse. They have included, for example, verbal recognition memory and both verbal and spatial working memory tasks [19,28], as well as visuospatial tasks like those in the present study [13]. Moreover, a variety of cortical areas have been reported to show increased activation including, for example, activation of homologous contralateral regions (in cases where activation is lateralized in young adults) as well as activation of areas of frontal cortex not activated in young adults ([19,28], for a review, see [14]). At the present time, it is unclear whether the increased activation in older adults reflects actual changes in how specific cortical structures process information or whether the increased activation reflects the acquisition of compensatory cognitive and behavioral strategies that are associated with activation of additional cortical areas (e.g. acquisition of strategies that involve spatial processing to assist in solving problems that previously relied primarily on shape processing). The latter possibility seems to us more likely, although it remains possible that other mechanisms are involved (e.g. greater integration of function). For the most part, however, the greater spread of activation in older adults has been seen as a form of recruitment that may serve to compensate for the age-related decline in neural functions [14,18,27], and the implicit assumption has been that recruited structures and processes are activated simultaneously with those activated in young adults. Brain areas that are heavily connected and that partially overlap in basic functions would seem to be likely candidates for such compensatory recruitment. For example, in the visual system, the interconnections between the ventral and the dorsal systems are quite extensive [35], and there are also numerous feedback and feedforward connections between the two visual streams and the prefrontal cortex [5,11]. Such interconnections may provide the structural basis for recruitment in response to injury or age-related decline in visuospatial functions. In conclusion, the present investigation of the structure of older adults visuospatial abilities revealed a dedifferentiation of the brain-based visuospatial ability factors that have been identified in young adults. Importantly, tasks constructed based on knowledge of the neurobiology of the visual system were used to assess visuospatial abilities. 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