Elsevier

Neurobiology of Aging

Volume 28, Issue 3, March 2007, Pages 459-476
Neurobiology of Aging

Adult age differences in the functional neuroanatomy of visual attention: A combined fMRI and DTI study

https://doi.org/10.1016/j.neurobiolaging.2006.01.005Get rights and content

Abstract

We combined measures from event-related functional magnetic resonance imaging (fMRI), diffusion tensor imaging (DTI), and cognitive performance (visual search response time) to test the hypotheses that differences between younger and older adults in top-down (goal-directed) attention would be related to cortical activation, and that white matter integrity as measured by DTI (fractional anisotropy, FA) would be a mediator of this age-related effect. Activation in frontal and parietal cortical regions was overall greater for older adults than for younger adults. The relation between activation and search performance supported the hypothesis of age differences in top-down attention. When the task involved top-down control (increased target predictability), performance was associated with frontoparietal activation for older adults, but with occipital (fusiform) activation for younger adults. White matter integrity (FA) exhibited an age-related decline that was more pronounced for anterior brain regions than for posterior regions, but white matter integrity did not specifically mediate the age-related increase in activation of the frontoparietal attentional network.

Introduction

Visual search and identification tasks engage multiple forms of attentional processing, including top-down (endogenous, cognitively driven) and bottom-up (exogenous, stimulus driven) components. The goal of both top-down and bottom-up processing is the guidance of attention to the search target [57], [78]. Behavioral studies of age-related cognitive change have reported a decline in attentional functioning in tasks involving visual search and target identification, especially when attention must be divided among multiple display items or input channels [38], [44]. Some degree of this age-related decline is a consequence of bottom-up deficits in the sensory and neural systems supporting the transmission of the visual signal [65], [66], [68]. Behavioral studies, however, have also identified some tasks in which there is an additional age-related decline in top-down attentional selection [16], [73], which may in turn represent a broader deficit in the executive control processes of coordinating, planning, and updating currently available information [71], [75], [76].

Current models of visuospatial attention, based on functional neuroimaging investigations of healthy younger adults, suggest that attentional processes are mediated by a widely distributed neural network, with critical components located in prefrontal, deep gray matter, and parietal regions [12], [18], [28], [31], [77]. There is in addition some differentiation within this frontoparietal network, comprising temporoparietal and inferior frontal cortex in the case of bottom-up attention, and dorsal parietal and superior frontal cortex in the case of top-down attention [13], [26], [56], [79]. The general theme of the neuroimaging results is that both frontal and parietal regions are sources of top-down attentional signals that modulate target detection activity in visual cortical regions, by raising the baseline activity for an attended object, counteracting the suppressive effects of surrounding distractors, and limiting the number of potential object representations [1], [14], [28], [67].

Neuroimaging studies of older adults have reported an extensive and complex pattern of age-related change in brain structure and function, including visual attention [9], [58]. The results suggest that age-related decline occurs in the task-related activation of visual sensory cortex, consistent with the behavioral evidence for age-related decline in the efficiency of bottom-up processing [40], [58]. In some tasks this decline is also accompanied by increased activation of other components of the frontoparietal attentional network, which has been interpreted as a compensatory recruitment of cortical regions outside the task-relevant pathway [8], [20]. Most often, the regions associated with increased activation for older adults have included dorsolateral prefrontal cortex [8], [21], [37], [45], [48], although age-related increases in the activation of deep gray matter structures [42] and parietal cortex [8], [21], [48] have also been observed.

Functional neuroimaging investigations of cognitive aging have been concerned primarily with the characterization and localization of age-related change in cortical function, that is, measures of cerebral metabolism and blood flow obtained from positron emission tomography (PET) and functional magnetic resonance imaging (fMRI). The cortical networks mediating cognitive function establish connectivity through white matter pathways, however, and localized changes in cortical activation within the attentional network (e.g., in the frontal lobes) may result from white matter changes at various points in the network [22], [61], [70].

Diffusion tensor imaging (DTI) provides information about the properties of white matter, by measuring both the rate and directionality of the displacement distribution of water molecules across tissue components [4], [32]. In DTI, one measure of white matter integrity is fractional anisotropy (FA), the degree to which water molecules diffuse in a single direction, which in turn is affected by axonal restrictions and myelin content. Fractional anisotropy tends to decrease as a function of increasing age, even in the absence of significant disease, suggesting a corresponding decline in the structural integrity of white matter with age that could compromise axonal conduction and the efficiency of information transfer among distributed cortical networks [46], [55]. Age-related decline in FA is typically more pronounced for anterior brain regions than for more posterior regions [24], [54], [62]. Independently of age, decreased white matter integrity is associated with lower performance on cognitive tasks [47], and this relation between white matter integrity and cognitive performance may in addition be altered as a function of age, in ways that are as yet not clear. The particular brain regions, for example, that exhibit an association between white matter integrity and cognitive performance may vary with age [41]. The disconnection of task-relevant cortical circuits by decreased white matter integrity has been proposed as a general mechanism of age-related decline in cognitive performance [2], [51], [52].

To date, however, we know of no published report in which DTI and fMRI measures have been combined, within participants, in the assessment of age-related change in cognitive function. The primary goal of this study was to take this first step, by conducting this combined assessment in the investigation of age-related changes in visual attention. We tested the hypothesis that age-related changes in attentional functioning would be related to cortical activation as measured by event-related fMRI, and that this relation, in turn, would be mediated by white matter integrity as measured by DTI.

We were interested specifically in the use of top-down attention during visual search. Previous neuroimaging studies of age differences in visual search using multi-item displays [36], [37] suggest that activation of visual processing (occipitotemporal) regions is greater for younger adults, whereas older adults exhibit relatively greater activation of the frontoparietal network. These previous studies, however, have not distinguished between top-down and bottom-up processing. Similarly, where age-related effects in top-down attentional control have been isolated, the experiments have used single-item displays that do not require the identification of a target item among distractors [42], [48]. We therefore used a multi-item search task in which we could isolate top-down attentional effects, by comparing blocks of trials in which the probability of a target-defining feature (color) is either relatively low (neutral condition) or relatively high (guided condition) [39], [43]. In addition, we adjusted the duration of the search displays between the age groups (while keeping the overall duration of visual stimulation constant), so that the influence of the age-related decline in bottom-up processing (i.e., occipitotemporal activation) would be less pronounced. Finally, with the aim of identifying network-dependent effects, we adopted a region of interest (ROI) approach in which we selected sets of gray matter ROIs likely to be critically involved in various aspects of visual search performance: frontal and parietal regions related to attentional and oculomotor control, deep gray matter regions related to sensory-motor integration and response initiation, and occipital regions related to visual sensory processing [12], [18], [28], [31], [77]. We generated white matter ROIs that target fiber systems coursing to and projecting from these gray matter regions.

We hypothesized that an age-related increase would occur in the magnitude of fMRI activation of the frontoparietal network [8], [20], and that this age difference would in turn be relatively greater in the guided condition, due to the top-down attentional control elicited by the higher level of target predictability. An age-related increase in the activation of deep gray matter regions has been associated with the type of motor responses required by this search task [42], and we predicted this type of age difference in the present task. In contrast, an age-related decline typically occurs in the activation of visual cortical regions [7], [36], [37], but our adjustment of display duration in this experiment would be expected to reduce this age effect. Critically, we predicted that the relation between the measures of neural activation and behavioral performance would change as a function of adult age. We reasoned that if an age-related increase in frontoparietal activation does occur, then this activation will be more highly correlated with search performance for older adults than for younger adults, and that younger adults would instead be more likely to exhibit a correlation between performance and activation in visual cortical regions [34], [37].

With regard to DTI, we predicted that an age-related decline in white matter integrity (as indexed by FA) would be evident, and that this decline would be more pronounced for anterior brain regions than for more posterior ones, as reported previously [24], [54], [62]. If, in addition, this age-related decline in white matter integrity is a mechanism of age-related neurocognitive change, then regression analyses should reveal that FA is related to age differences in fMRI activation. More specifically, from the perspective of a disconnection theory [2], [51], [52], we would expect that FA would correlate with fMRI activation and, further, be a mediator of the relation between fMRI activation and visual search performance. Accordingly, the statistical control of individual differences in FA should lead to a decrease in the relation between activation and performance, especially within the frontoparietal network, and this mediating role of FA should be more clearly evident for older adults than for younger adults. Thus, our overall goal was to establish whether age-related change in cortical activation was associated specifically with top-down guidance during visual search, and to determine whether a disconnection model of white matter integrity could account for the age-related changes in activation.

Section snippets

Participants

The Institutional Review Board of the Duke University Medical Center approved the research procedures, and all participants gave written informed consent. The participants were 16 younger adults (8 women) between 19 and 28 years of age (M = 23.4 years) and 16 older adults (8 women) between 60 and 82 years of age (M = 67.0 years). All participants were right-handed, community-dwelling individuals. Younger adults and older adults did not differ significantly with regard to the number of years of

Visual search performance

Response time and error rate in the visual search task are presented in Table 3. Error rate was low and did not differ significantly as a function of age group (younger adults M = 2%; older adults M = 1%). In the analysis of RT for correct responses, we obtained the median RT for each participant in each combination of task condition and target type. Univariate analysis of variance (ANOVA) conducted on these RT data, with the between-subjects variable of age group and the within-subjects variables

Discussion

In this research we combined behavioral data from visual search performance, cortical activation from event-related fMRI, and white matter integrity from DTI, to investigate age-related changes in the functional neuroanatomy of visual attention. On the basis of previous findings, we predicted that activation in a frontoparietal network would be greater for older adults than for younger adults, especially when the task required top-down attentional control. We also expected that the regional

Conclusion

The functional neuroanatomy of visual attention comprises both age-independent and age-related effects. Independently of adult age, posterior regions of the attentional network (angular gyrus and superior parietal lobule) are activated by top-down attention, when there is a high proportion of trials on which a salient visual feature (a color singleton) can be used to guide attention to a search target. Within this guided condition, on singleton-target trials, there is an age-related difference

Acknowledgements

This research was supported by grants R01 AG11622, R01 AG19731, R37 AG002163, and T32 AG00029, from the National Institute on Aging. We are grateful for assistance from Susanne Harris, Leslie Crandell Dawes, and Sara Moore.

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