تفاوت مربوط به سن در مشارکت قشر جلوی مغز در کنترل توجه

Abstract We investigated the relative involvement of cortical regions supporting attentional control in older and younger adults during performance on a modified version of the Stroop task. Participants were exposed to two different types of incongruent trials. One of these, an incongruent-ineligible condition, produces conflict at the non-response level, while the second, an incongruent-eligible condition, produces conflict at both non-response and response levels of information processing. Greater attentional control is needed to perform the incongruent-eligible condition compared to other conditions. We examined the cortical recruitment associated with this task in an event-related functional magnetic resonance imaging paradigm in 25 older and 25 younger adults. Our results indicated that while younger adults demonstrated an increase in the activation of cortical regions responsible for maintaining attentional control in response to increased levels of conflict, such sensitivity and flexibility of the cortical regions to increased attentional control demands was absent in older adults. These results suggest a limitation in older adults’ capabilities for flexibly recruiting the attentional network in response to increasing attentional demands.

Introduction Representations arising from distracting stimuli interfere with our ability to selectively attend to task-relevant information. The effect of such representations is heightened when the tendency to respond to distracting information is habitual or reflexive, resulting in the need for greater attentional control to perform important tasks. The classic color-word Stroop task has been extensively used in both the behavioral and neuroimaging literatures to study the mechanisms of attentional control (Banich et al., 2000, Banich et al., 2001, Bench et al., 1993 and Desimone and Duncan, 1995). In the Stroop task, participants are asked to inhibit information from the pre-potent word representations and attend to the color in which the words are printed. Heightened attentional control is needed to resolve the interference on trials in which the color and word information are incongruent (e.g. the word ‘BLUE’ printed in red ink) compared to conditions in which the color and word information are not conflicting. Young adults during performance of the incongruent trials activate a network of regions including the bilateral middle frontal gyrus, bilateral inferior frontal gyrus, anterior cingulate cortex (ACC) and the parietal cortex (Banich et al., 2001 and Bench et al., 1993) due to increased attentional control required to overcome the task-irrelevant dimensions of the incongruent condition. Older adults, in comparison to young adults, are thought to have deficits in their ability to selectively attend to and ignore irrelevant information (see Hasher & Zacks, 1988; Kramer, Humphrey, Larish, Logan, & Strayer, 1994). For example, older adults often show performance deficits on the Stroop task, which is considered to be indicative of an age-related inability to effectively filter the task-irrelevant (word) information. Neuroimaging research has demonstrated increased recruitment of brain regions by older adults to perform cognitive tasks in which younger adults more selectively recruit neural resources (Cabeza et al., 2004, Colcombe et al., 2005 and Langenecker et al., 2004). This increased recruitment of brain regions has been interpreted in a number of different ways with some researchers suggesting a compensatory role performed by the additional activation to counter the declines associated with advancing age. For example, Langenecker et al. (2004), using the Stroop task found that older adults showed more activation than younger adults in the premotor, dorsolateral, ventrolateral and medial frontal areas. Particularly, the study reported greater activation in the left inferior frontal regions by the older participants, thus arguing for the task-specific and supportive role of this region to overcome the greater interference experienced by older adults. Though this study did not report correlations between additional activation and behavioral performance, other studies (Cabeza et al., 2004 and Reuter-Lorenz et al., 2000) using a variety of cognitive tasks have reported positive correlations between increased activation and behavioral performance in older adults. The additional recruitment of cortical resources by the better performing subgroup has been interpreted as compensatory processing, serving to deal with, at least in part, age-related inefficiencies in processing associated with different tasks. Though a compensatory interpretation of additional activation in the presence of declining neural efficiency has some support, the recruitment of more cortical resources on relatively easy tasks might have hidden costs (Reuter-Lorenz & Lustig, 2005; Reuter-Lorenz & Mikels, 2006). Reuter-Lorenz and Mikels (2006) proposed that as a result of the need to allocate substantial cortical resources to tasks that younger adults find relatively easy, older adults have few resources available for more challenging tasks. This pattern of results has been termed the CRUNCH model or the compensation-related utilization of neural circuits hypothesis. According to this hypothesis, older adults show less of a difference compared with younger adults in the activation between two tasks or conditions that differ in difficulty. It is possible that such a finding would represent an age-related failure to flexibly allocate cortical resources with increasing task demands (see DiGirolamo et al. (2001) for a similar hypothesis). In this study, we manipulated the level of conflict in the incongruent conditions of the Stroop task (Milhalm et al., 2001 and Liu et al., 2006) to examine differential recruitment of brain regions in both young and old participants. We presented a modified version of the Stroop task to our participants: older adults between 58 and 75 years of age, and younger adults between 18 and 35 years of age. In addition to the neutral (the word LAMP printed in red ink) and the congruent (the word RED printed in red ink) conditions we had two types of incongruent conditions (incongruent-eligible and incongruent-ineligible) enabling us to further study the effect of increases in conflict on behavioral performance and brain processes in younger and older adults. The paradigm was a three-choice manual response task, in which participants were asked to respond to the three ink colors (red, green or purple) using their right hand. An incongruent-eligible stimulus was one of the words from the set of colors that the participant could respond with (red, green or purple) printed in an incongruent ink-color (e.g. the word RED printed in green ink). An incongruent-ineligible stimulus, in contrast, was any color-word other than red, green or purple printed in an incongruent color (e.g. the word BLUE printed in green ink). For both these trials, the participants were asked to make responses (see Fig. 1 for a pictorial representation of the task). The main difference between the two incongruent conditions was that in the eligible condition the actual color-word was a part of the response set with which the participant could respond and hence greater response conflict. In the ineligible trials, the color-word was not a part of the response set. Pictorial representation of the modified version of the Stroop task used in the ... Fig. 1. Pictorial representation of the modified version of the Stroop task used in the study. Participants could only respond to three ink colors: red, green or purple. For the incongruent-eligible condition (third box) the word was one of the ink colors that the participant could respond with (red, green or purple) but printed in an incongruent ink-color (such as GREEN printed in red ink). For the incongruent-ineligible condition (fourth box), the word could be any color-word other than red, green or purple printed in an incongruent ink-color (such as the word BLUE printed in red ink). Figure options Milhalm et al. (2001) employed this paradigm to investigate attentional control in young adults. They reported that young adults activated primarily the left prefrontal cortex during the incongruent-ineligible condition relative to the neutral condition. Performance on the incongruent-eligible trials relative to neutral trials resulted in greater activation in the left PFC along with additional activation in the right PFC and anterior cingulate cortex. The authors conceptualized the additional activation during the incongruent-eligible condition as being reflective of the differences in the amount of conflict experienced in the two tasks. That is, the incongruent-ineligible condition was thought to involve non-response conflict given that the word was not a part of the response set, while the incongruent-eligible condition was hypothesized to involve both response and non-response conflict. Through this manipulation, we were interested in examining whether older adults have a reduced capability to flexibly allocate attentional resources. We used an event-related functional magnetic resonance imaging (fMRI) paradigm to investigate the recruitment of the prefrontal and parietal cortices in older adults in response to increased attentional demands on this version of the Stroop task. Previous studies using the traditional Stroop task have examined age-related differences in attentional control (see Langenecker et al., 2004; Milhalm et al., 2002) and in this study, in addition to examining cortical recruitment during the incongruent condition relative to the neutral condition, we examined the neural circuitry recruited by the older adults compared with the younger adults during the two incongruent conditions. This enables a unique comparison of the neural resources utilized by the two groups in response to increasing cognitive demands. We predicted that the older adults would demonstrate increased activation of the cortical resources in response to all conditions of the Stroop task, such that cortical resources recruited by the younger adults during the more challenging incongruent conditions would be recruited by older adults in response to the congruent and the neutral condition. In addition, we also predicted that older adults would recruit bilateral areas of the dorsolateral prefrontal cortex in response to the easier task condition (incongruent-ineligible), thereby leaving no additional resources for the more challenging condition (i.e. incongruent-eligible). In other words, as opposed to younger participants who would demonstrate an increase in activation in response to increases in conflict between the incompatible conditions, older adults would recruit similar brain regions in response to easier task conditions, supporting the claim that older adults have more difficulty flexibly and adaptively recruiting neural resources to assist task performance.

. Results 3.1. Behavioral results 3.1.1. Reaction time Reaction time (RT) and accuracy rates of all participants were recorded while they performed the Stroop task in the scanner (Table 1). For reaction time analyses, only RT’s for correct trials were included. The results from the repeated measures analysis of variance with condition (congruent, neutral, incongruent-eligible and incongruent-ineligible) as a within-subjects factor and age as a between-subjects factor revealed a main effect of age (F(1, 48) = 47.81, p < 0.001). These effects indicate that older adults were slower than younger adults. The main effect of condition (F(1, 48) = 43.98, p < 0.0001) and the interaction of age X condition were also significant (F(1, 48) = 2.70, p < 0.05), such that older adults showed a greater increase in RT for incongruent-eligible trials relative to the neutral and the incongruent-ineligible trials than younger adults. Post-hoc paired t-tests between different conditions indicated that there was a significant difference between the incongruent-eligible condition and the neutral condition, congruent condition and the incongruent-ineligible condition for both the young and the older groups of participants; the difference, however, was much more pronounced for the older adults. These results thus suggest that the incongruent-eligible condition resulted in significant conflict for both groups of participants, relative to the other conditions. Table 1. Reaction time and error rates (expressed as %) for old and young adults. Standard errors are included in parentheses. Congruent Neutral Incongruent-eligible Incongruent-ineligible Old Reaction time 822.56 (15.3) 825.48 (17.6) 913.20 (21.03) 883.08 (19.67) Error rates 2.56 (0.59) 2.23 (0.55) 6.44 (1.36) 3.34 (0.76) Young Reaction time 656.57 (16.03) 676.08 (18.86) 727.16 (21.90) 706.02 (18.05) Error rates 2.33 (1.38) 4.00 (1.87) 4.89 (1.60) 4.11 (1.15) Table options 3.1.2. Accuracy Similar to the RT data, accuracy data was analyzed using a repeated measures ANOVA. We found a main effect of condition (F(1, 48) = 6.33, p < 0.001), however, the main effect of age and the age X condition interaction were not significant. Consistent with the RT data, paired t-tests indicated a significant difference between the error rates on the incongruent-eligible condition and the congruent, neutral and the incongruent-ineligible condition for the older adults. For younger adults, we found a significant difference between error rates of the incongruent-eligible condition and the congruent condition. 3.2. Neuroimaging results 3.2.1. Main Stroop effect Collapsing across the two incongruent conditions, we found that the younger adults activated bilateral areas of the prefrontal cortex, left superior parietal lobules as well as the bilateral occipital cortices during the incongruent trials relative to the neutral trials (Fig. 2B and Table 2B). Activation in the neutral condition was restricted to the parietal and occipital lobules, however, with an increase in the level of conflict, younger adults demonstrated a greater recruitment of the prefrontal regions (Fig. 3). In contrast, we found that the older adults primarily recruited the left middle frontal gyrus, and the left superior parietal lobule in response to the incongruent > neutral contrast (Fig. 2A and Table 2A). Fig. 3 also shows activation in the congruent, neutral and the two incongruent conditions for the older and younger adults. As can be seen from the figure, for both the congruent and the neutral trials, older adults demonstrated significant activation in the prefrontal cortices. Represents activation in the incongruent>neutral contrast for both groups of ... Fig. 2. Represents activation in the incongruent > neutral contrast for both groups of participants. The last row represents the inclusive mask generated for investigating differential recruitment patterns in the two groups as a function of task difficulty. Figure options Table 2. Local maxima in the incongruent > neutral contrast for (A) older adults and (B) younger adults. Region Peak z-stat MNI(X) MNI(Y) MNI(Z) (A) Cuneus (R) 2.80 12 −96 22 Inferior frontal gyrus (L) 3.39 −42 3 35 Inferior parietal lobule (L) 3.38 −36 −68 43 Middle frontal gyrus (L) 3.48 −55 19 34 Precuneus (L) 3.94 −6 −78 42 Supramarginal gyrus (L) 3.22 −48 −61 32 (B) Fusiform gyrus (L) 3.28 −22 −72 −19 Inferior frontal gyrus (L) 3.68 −48 7 29 Inferior frontal gyrus (R) 3.43 48 11 20 Inferior parietal lobule (L) 3.92 −51 −37 42 Insula (L) 3.21 −32 20 5 Insula (R) 3.81 40 14 3 Lingual gyrus (L) 4.00 −8 −87 −9 Lingual gyrus (R) 3.20 12 −82 −18 Precuneus (L) 3.52 −26 −72 42 Posterior cingulate (R) 3.08 14 −71 7 Superior parietal lobule (L) 4.09 −14 −75 62 Supramarginal gyrus (L) 3.37 −65 −51 32 Table options Cortical recruitment in the four conditions of the Stroop task. Fig. 3. Cortical recruitment in the four conditions of the Stroop task. Figure options 3.2.2. Eligibility manipulation In order to examine age differences in the recruitment of cortical resources and their subsequent manipulation as a function of task difficulty, we created an inclusive mask for the incongruent > neutral contrast by collapsing across age groups (Fig. 2C). We then created ROIs based on the clusters identified in the collapsed incongruent > neutral contrast to examine modulation of the prefrontal and the parietal regions in response to increasing task demands for both older and younger participants. Fig. 4 represents the average percent signal change in the ROIs identified through the incongruent > neutral contrast for all conditions of the Stroop task. These ROIs comprising of bilateral MFG, bilateral areas of the parietal lobules and the precuneus demonstrated interesting patterns of recruitment for the two age groups. For both clusters in the prefrontal cortex (Fig. 4A and B), older adults demonstrated either significantly greater activation than younger adults or a trend towards greater activation in the different conditions (with the exception of the incongruent-eligible condition). This is consistent with previous research reporting increased activation in older adults in response to different cognitive tasks (Cabeza et al., 2004 and Colcombe et al., 2005). Consistent with our hypothesis, we found that younger adults demonstrated an increase in the recruitment of the right MFG in response to increasing task demands, reflected by increased activation in the incongruent-eligible condition relative to incongruent-ineligible condition (t = 2.035, p < 0.05). In comparison, older adults failed to show such a modulation (t = 1.26, ns) of the right PFC in response to increasing task demands. Though older adults did demonstrate an increase in the recruitment of right MFG for the incongruent-eligible and the ineligible condition relative to the neutral and congruent conditions, the increase was more pronounced for younger adults ( Fig. 4). Similarly for the left MFG, older adults demonstrated no difference between the two incongruent conditions, while younger adults showed a marginally significant difference (t = 1.92, p = 0.06) between the two incongruent conditions. The difference between the incongruent conditions and the congruent and neutral conditions was again much more pronounced for younger adults relative to older adults ( Fig. 4). These results thus suggest that older adults do have difficulty in flexibly recruiting of the prefrontal cortices in response to increases in task demands. Full-size image (90 K) Fig. 4. Represents percent signal change in the ROIs identified through the incongruent > neutral contrast in the four conditions of the Stroop task. (A) Activation in the right MFG for older and younger adults. As predicted, younger adults show a greater recruitment of the right MFG in response to the incongruent-eligible condition relative to the incongruent-ineligible condition. Older adults, failed to show such a modulation of the right MFG. * Represents significance at p < 0.05. (B) Activation in the left MFG for older and young participants. There was a marginally significant different (p = 0.06) between the two incongruent conditions for the younger adults. The recruitment of the left MFG was not significantly different between the two incongruent conditions for the older adults. * Represents significance at p < 0.05. (C) Activation in the right parietal for both groups of participants. Both groups of participants showed a greater activation of the right parietal lobule during the incongruent trials as compared to the congruent and the neutral trials. (D) Activation in the left parietal for both groups. Difference between the two incongruent conditions was not significant for either group of participants. (E) Activation in the precuneus/lateral occipital cortex for both groups of participants. Cortical recruitment in this area for both groups did not differ for the two incongruent conditions. * Represents significance at p < 0.05. Figure options In contrast, for the parietal regions and the precuneus, both older adults and younger adults failed to show a difference in activation between the two incongruent conditions of the Stroop task. Younger adults did show a significant increase in the recruitment of the bilateral parietal cortices and the precuneus during the incongruent-eligible condition relative to the congruent and the neutral conditions (p < 0.05 for all paired t-tests conducted for the three cortical regions). During the incongruent-ineligible condition, they demonstrated a similar increase in the recruitment of the right parietal and the precuneus relative to the congruent and the neutral conditions (p < 0.05), however, the increase in the left parietal cortex during the incongruent-ineligible condition was marginally significant (p = 0.09 relative to the neutral condition). Older adults, also demonstrated an increase in the recruitment of the left parietal and the precuneus during the incongruent-eligible relative to the neutral and the congruent conditions (p < 0.05), however, for the right parietal this difference was only marginally significant (p = 0.09). For the incongruent-ineligible condition, they demonstrated an increase in the left and the right parietal cortices (p < 0.05) relative to the neutral condition, however, the difference was not significant for the precuneus ( Fig. 4C–E).