Elderly adults through compensatory responses can be just as capable as young adults in inhibiting the flanker influence

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Abstract

The goals of this study were to determine whether there is an age-related flanker effect, whether elderly adults produce compensatory responses to overcome their deficiencies, and the extent to which any compensatory responses vary depending on the degree of task demands. To achieve these goals, we manipulated different degrees of demands in cognitive control in a flanker-task paradigm, such as by arranging different proportions of trials in which either a compatible or an incompatible response with respect to the target's pointing direction was required. Throughout the three experiments, we did not observe an increased flanker effect on behavioral measures exhibited by elderly adults compared with young adults. However, several compensatory responses by elderly adults were observed, as evident by the results of event-related potential components. Furthermore, these age-related compensatory responses did not vary as a function of different degrees of task demands. The results suggest that, through the use of compensatory responses, elderly adults are just as capable as young adults in inhibiting flanker influence.

Highlights

► This study manipulated different degrees of demands in cognitive control. ► Older adults did not show an increased flanker effect on behavioral measures. ► Older adults through compensatory mechanisms can overcome the flanker interference.

Introduction

Many cognitive functions deteriorate with age, which leads to reductions in perceptual processing speed (Madden, 2001, Salthouse, 1994, Salthouse, 1996), diminished working memory capacity (Grady and Craik, 2000, Salthouse, 1994, West, 1996), deficits in inhibitory processing (Hasher and Zacks, 1988, Kramer et al., 1994), and decreased cognitive flexibility (Kramer et al., 1999, Mayr, 2001). These cognitive dysfunctions have been linked to a decline in brain function in the elderly, and the prefrontal cortex has been generally believed to be the brain region that is most affected by aging (Dempster, 1992, Dennis and Cabeza, 2008, Raz, 2000, West, 1996). The frontal hypothesis of cognitive aging has proposed that elderly adults do not perform as well as young adults on cognitive control tasks because these tasks depend on frontal lobe function.

However, in contrast to the common view that elderly adults are inevitably inferior to young adults in regulating cognitive control, some researchers have identified an important compensatory mechanism that elderly adults employ to mitigate performance deficiencies (Cabeza et al., 2002, Phillips and Andrés, 2010, Park and Reuter-Lorenz, 2009, Reuter-Lorenz and Cappell, 2008). Phillips and Andrés (2010) have noted that although older and younger adults can perform at the same behavioral level in some cognitive tasks, the two groups may exhibit different patterns of underlying brain activity due to the different strategies adopted by older adults. In addition, researchers have found that task characteristics, such as the type of task and task demands, modulate cognitive aging effects (Humphrey and Kramer, 1997, Kramer et al., 1994, McLaughlin et al., 2010). For example, McLaughlin et al. (2010) observed that age-related changes in spatial selective attention were influenced by task demands and the types of attention measures used. Moreover, age-related compensatory brain responses may be influenced by task demands in complex ways (Cappell et al., 2010, Rajah et al., 2010, Vallesi et al., 2010). For example, Vallesi et al. (2010) demonstrated that older adults’ compensatory brain responses engaged the more extensive fronto-parietal brain network to overcome a prepotent and inappropriate response only when the task was more complex and novel. In contrast, however, an earlier study (Eppinger et al., 2007) investigated adaptation to changing task contexts that varied the ratio of incongruent to congruent Stroop stimulus trials and found no effect of the ratio in older adults, which demonstrated impaired flexibility in the older group and suggested that older adults were less able to develop expectancies regarding stimulus congruency. Hence, Eppinger et al.’s (2007) findings suggest that the elderly might employ all-or-none compensatory responses that are insensitive to the degree of task difficulty.

It is not surprising to find conflicting results regarding the effect of age on cognitive control functions due to the many possible moderators. For example, previous laboratory studies of the ability to inhibit distractor interference have shown that elderly adults are more susceptible than younger adults to interference due to distraction and irrelevant stimulus information (for an overview, see Guerreiro et al., 2010 and Kok, 1999). The widely known age-related inhibitory deficit theory has been proposed to account for older adults’ increased susceptibility to distractors (Hasher and Zacks, 1988, Hasher, 2007). However, a closer examination of the literature reveals that the general theory of age-related inhibitory deficit has received mixed support from empirical studies using the Eriksen flanker task (Eriksen and Eriksen, 1974). Participants in a conventional flanker task are required to respond to a centrally positioned target and ignore simultaneously presented distractors that flank the target, and the flanking distractors are either associated with a response that is congruent to the target, in conflict with the target, or neutral. While some studies have demonstrated that older adults are less able to inhibit flanker interference, which supports inhibitory deficit theory (Colcombe et al., 2005, Machado et al., 2009, Shaw, 1991, Zeef and Kok, 1993, Zeef et al., 1996), some studies of the flanker interference effect have failed to find significant differences between younger and older adults (Falkenstein et al., 2001, Fernandez-Duque and Black, 2006, Gunter et al., 1996, Jennings et al., 2007, Kramer et al., 1994, Madden and Gottlob, 1997, Nieuwenhuis et al., 2002, Wild-Wall et al., 2008), whereas others have found the opposite pattern in which older adults exhibit less interference than younger adults (Kamijo et al., 2009, Madden and Gottlob, 1997, Mathewson et al., 2005; for a more comprehensive review, see Guerreiro et al., 2010). Hence, some mediating factors may not yet have been identified.

Wild-Wall et al. (2008) explored the factors contributing to these contradictory findings and discovered that older adults might resolve the conflicting information in a flanker task by adopting a strategic, top–down enhancement of visual processing of the central targets and of the response threshold that emphasizes performance accuracy (see also Zeef et al., 1996). However, because follow-up studies have yet to directly determine whether elderly adults employ compensatory responses, further empirical investigation of the phenomenon is needed. Because Wild-Wall et al. (2008) did not identify the conditions that lead the older adults to employ effective compensatory responses in a flanker task, the present study addressed this issue.

The goals of this study were to determine whether there is an age-related flanker effect, whether elderly adults produce compensatory responses to overcome their deficiencies (Wild-Wall et al., 2008), and the extent to which any compensatory responses vary depending on the degree of task demands. To address these issues, this study used event-related potential (ERP) methodology, which yields high temporal resolution and direct observations of the changes in the brain activities during sensory, cognitive, and motor stages of processing. The ERP findings revealed the underlying brain compensatory responses that promoted older adults’ behavioral performance in a flanker task and the extent to which these brain compensatory responses were modulated by task demands.

To manipulate the demands of the task, the flanker-task paradigm was modified by introducing a color-coded target, and different target colors represented either a compatible (PRO) response or an incompatible (ANTI) response (Van’t Ent, 2002). Participants responded to the color associated with the PRO condition by using the hand that corresponded to the direction of the target arrow and responded to the different color associated with the ANTI condition by using the hand that corresponded to the direction opposite to the target arrow. Previous research has reported an increased error rate and slower reaction time (RT) in the ANTI condition (Doucet and Stelmack, 1999, McCarthy and Donchin, 1981, Nessler et al., 2007). Furthermore, Nessler et al. (2007) also found that the differences in RT and the error rate were greater for the elderly group than for the young adult group in the ANTI condition, indicating that the elderly found the ANTI condition to be more demanding. In the present study, the proportion of PRO and ANTI trials was manipulated to bias participants’ expectations regarding the type of target. Although the presence of ANTI trials in the flanker task alone might be sufficient to induce older adults’ compensatory responses regardless of the probability of this type of trial, a certain proportion of ANTI trials to total trials might be required to reach a task demand threshold that evokes compensatory responses. We hypothesized that as the probability of ANTI trials in a block increased, the task difficulty would increase as well. To determine whether there was a task demand threshold that induced compensatory responses in the elderly, the proportion of ANTI trials was manipulated to precisely vary the extent of the demands on cognitive control.

To investigate the ERP correlates of the flanker effect and possible compensatory responses, this study examined several relevant ERP components. Because the stimulus-locked N1 over the occipital scalp regions is held to reflect sustained covert visual attention (Di Russo et al., 2003), the amplitude of the N1, which is time-locked to the onset of a central target, may be associated with the intensity of covert attention to the central target in a flanker task. As a result, N1 amplitude might indicate whether elderly adults adopt the control strategy of increasing visual attention to the central target (Wild-Wall et al., 2008).

The stimulus-locked frontal N2 component, which peaks 300 ms after the stimulus onset, has been found to be present on incongruent trials but not on congruent trials, and N2 magnitude has been found to be positively associated with the extent of the response conflict due to flanker interference (Botvinick et al., 2001, Kopp et al., 1996, Nieuwenhuis et al., 2003, Van Veen and Carter, 2002a, Van Veen and Carter, 2002b). Hence, by observing the extent to which the stimulus-locked frontal N2 is modulated by age and/or different levels of task difficulty, it is possible to determine whether older adults experience more flanker conflict than younger adults due to inhibitory function deficits (i.e., increased N2), or experience less conflict due to compensatory responses (i.e., decreased N2).

The stimulus-locked parietal P3b was also of interest because its peak latency has been held to reflect processing speed or the ease with which evaluative categorization occurs (Kutas et al., 1977, Luck, 1998). Hence, by observing if the P3b peak latency differs based on age and/or different levels of task difficulty, we can determine whether the elderly adopt a strategy of increasing attention to the central target and the extent to which such a strategy interacts with the PRO/ANTI condition and/or the level of task demands.

Two other response-locked ERP components—error-related negativities (ERN) and correct-related negativity (CRN)—were also relevant. These two components, which are often examined in flanker tasks, are thought to reflect response-related monitoring processes. The ERN is an ERP component that occurs after the commission of errors in speeded reaction tasks (Falkenstein et al., 1991, Gehring et al., 1993) and peaks 60–100 ms after an error response with maximal frontal–central distribution. Originally, the ERN was thought to reflect error detection, but a growing body of research has suggested that the ERN is involved in a more general evaluation of action plans (Luu et al., 2000, Vidal et al., 2000) or in the estimation of the motivational value of ongoing events (Bush et al., 2000, Pailing and Segalowitz, 2004, Hajcak et al., 2005). Because emphasizing accuracy might induce a larger ERN by making errors more salient and important (Gehring et al., 1993, Hajcak et al., 2005), we hypothesized that if older adults adopted the compensatory strategy of emphasizing performance accuracy, they would exhibit an equivalent or even larger ERN compared to younger adults.

In addition to the ERN, researchers have found that many individuals also exhibit a response-locked fronto-central negativity associated with the execution of correct responses, which is termed correct-related negativity (CRN; Ford, 1999, Mathalon et al., 2002). The CRN has been demonstrated to reflect either partial error processing on correct trials due to uncertainty about the response correctness (Coles et al., 2001, Pailing and Segalowitz, 2004, Vidal et al., 2000, Vidal et al., 2003), or, alternatively, a sensitivity to response strategy selection that is independent of error detection (Bartholow et al., 2005). Bartholow et al. (2005) have shown that the CRN amplitude was influenced by the manipulation of the probability of congruent and incongruent trials and that it was elicited when expectancies regarding stimulus congruency were violated. Schreiber et al. (2011) further demonstrated that older adults exhibited both decreased ERN amplitude, which indicated reduced error monitoring, and increased CRN, which indicated increased strategic monitoring. Thus, we hypothesized that older adults who engaged in a strategic control process would exhibit an increased CRN compared to younger adults.

In summary, we hypothesized that older adults who engaged in compensatory responses when performing a flanker task would exhibit increased performance accuracy and an unimpaired RT flanker effect as well as changes in the relevant ERP components described above. We also examined whether older adults’ compensatory responses varied as a function of task difficulty, or, alternatively, occurred in an all-or-none fashion despite differences in task demands.

Section snippets

Overview of experiments 1–31

The three experiments performed in the study employed identical stimuli, procedures, and designs, but the proportion of PRO and ANTI trials differed in each experiment. To directly compare the results of the three experiments, a 4-way mixed analysis of variance (ANOVA) with the between-subject factors of experiment (Experiment 1 = PRO-bias, Experiment 2 = non-bias, Experiment 3 = ANTI-bias) and age group (young, old) and the within-subject factors of trial condition (PRO, ANTI) and flanker type

Behavioral data

Trials with reaction times (RTs) that were less than 100 ms or greater than 3000 ms were rejected. For Experiments 1–3, the omission error rates for the younger group averaged 0.47%, 0.36%, and 0.97%, respectively, and the omission error rates for the older group averaged 1.08%, 1.23%, and 1.19%, respectively. Because data screening tests indicated that the data did not violate the assumption of normality, the RT and response accuracy data across all trials and the three experiments were analyzed

Discussion

The goals of this study were to determine whether there were age-related increases in the flanker effect, if elderly adults employed compensatory responses to overcome their deficiencies in flanker tasks, and whether compensatory responses were modified due to increasing task demands. For the three experiments in this study, which exhibited three different levels of task demands based on different ratios of response-incompatible (ANTI) to compatible (PRO) trials, the RT of older adults did not

Conclusions

Throughout the three experiments, we did not observe an age-related increase in flanker effect on behavioral RT measures. However, the older adults exhibited several compensatory responses. This was evident from the greater overall accuracy of performance and decreased flanker effect on accuracy as well as from age-related modulations on several ERP components. These age-related modulations include increased N1 to the central target, decreased N2 to incongruent trials, prolonged P3b peak

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