Elsevier

NeuroImage

Volume 91, 1 May 2014, Pages 52-62
NeuroImage

Brain mechanisms underlying the effects of aging on different aspects of selective attention

https://doi.org/10.1016/j.neuroimage.2014.01.029Get rights and content

Highlights

  • Attention concerns both enhancement and suppression of information.

  • Aging has differential effects on these aspects of attention.

  • We examined the neural underpinnings of these differential aging effects.

  • Older adults engage additional cognitive control to enhance performance.

Abstract

The ability to suppress irrelevant information declines with age, while the ability to enhance relevant information remains largely intact. We examined mechanisms behind this dissociation in an fMRI study, using a selective attention task in which relevant and irrelevant information appeared simultaneously. Slowing of response times due to distraction by irrelevant targets was larger in older than younger participants. Increased distraction was related to larger increases in activity and connectivity in areas of the dorsal attention network, indicating a more pronounced (re-)orientation of attention. The decreases in accuracy in target compared to nontarget trials were smaller in older compared to younger participants. In older adults we found increased recruitment of areas in the fronto-parietal control network (FPCN) during target detection. Moreover, older adults showed increased connectivity between the FPCN, supporting cognitive control, and somatomotor areas implicated in response selection and execution. This connectivity increase was related to improved target detection, suggesting that older adults engage additional cognitive control, which might enable the observed intact performance in detecting and responding to target stimuli.

Introduction

Every second, the human retina can send around 10 million bits of information to the brain (Koch et al., 2006). With such enormous quantities of information, the selection of behaviorally relevant pieces of information is essential. Two separate top–down modulatory mechanisms have been suggested to underlie selection of relevant information; suppression of irrelevant information and enhancement of relevant information (Gazzaley et al., 2005, Hillyard et al., 1998).

Aging affects selective attention. Previous research has shown that task performance in older adults is especially affected by the presence of irrelevant stimuli compared to younger adults (de Fockert et al., 2009, Haring et al., 2013, Mager et al., 2007, Schmitz et al., 2010). This is reflected in increased slowing of response times when participants are presented with distracting stimuli (Geerligs et al., 2012b). Using a working memory paradigm, in which to be remembered and to be forgotten information was presented sequentially, the Gazzaley group showed that older adults indeed had trouble suppressing irrelevant information, whereas enhancement of relevant information was found to be intact (e.g. Gazzaley et al., 2005, Gazzaley et al., 2008; for a review see Gazzaley, 2011). Moreover, they found that the decreased ability to suppress irrelevant information was related to decreased memory capacity for relevant information (Gazzaley et al., 2008).

It should be noted that not all studies have found a deficit in the suppression of irrelevant information with age (e.g. Kramer et al., 1994, Wild-Wall et al., 2008). It has been suggested that enhancement of relevant stimuli might actually be amplified in older compared to younger participants to overcome the age-related deficits in suppression (Haring et al., 2013, Wild-Wall et al., 2008). However, it has also been shown that under higher levels of visual load, that is in the context of distracting information, older adults do have trouble enhancing relevant stimuli (Chee et al., 2006). Quigley et al. (2010), for example, instructed participants to detect the direction of motion in a cloud of dots, all in one color. In addition, they superimposed another cloud of dots in a different color that acted as distractors. A cue indicated which color participants should attend to. Using an EEG technique (frequency tagging), the authors showed that younger adults clearly enhanced processing of stimuli with a relevant color. Older adults, however, showed no enhancement of relevant stimuli with respect to the pre-cue period and were significantly less accurate than young adults in detecting coherent motion. This suggests that when relevant and irrelevant information is present simultaneously, older adults can have trouble enhancing relevant information. It has been shown that declines in the visual system can cause deficits in the detection of briefly presented stimuli (e.g. Eriksen et al., 1970). However, as the stimuli in the Quigley et al. (2010) study were presented for a long period of time (2.2 s), this is unlikely to be the cause of the deficit in enhancement.

Top–down modulation of visual stimulus processing relies on a network of frontal and parietal brain regions, the dorsal attention network (DAN), operating in close interaction with the sensory cortices (Corbetta and Shulman, 2002, Desimone and Duncan, 1995, Kastner and Ungerleider, 2000). The main components of this DAN are the frontal eye fields (FEF) and the superior parietal lobule (SPL). Signals from these areas cause changes in the baseline firing rates of neurons and neural synchronization, leading to a larger neural responsiveness in the sensory cortices when a stimulus is attended (Reynolds and Chelazzi, 2004). This increased neural responsiveness is visible in the increased amplitude of early event related potentials (ERPs) and increased blood oxygen level-dependent (BOLD) signals for attended stimuli (Gazzaley et al., 2005, Hillyard et al., 1998) and leads to an increased ability to detect stimuli with attended spatial or non-spatial features. For unattended stimuli the opposite pattern emerges; neural responsiveness is reduced leading to decreased stimulus detection.

The mechanism described above allows segregation of relevant from irrelevant information in perceptual stages of processing. This requires that previous knowledge on the features or locations of relevant information and the task goals is maintained in working memory, involving activation of the fronto-parietal control network (FPCN). This network consists of the dorsolateral prefrontal cortex (DLPFC), the inferior and superior parietal cortex, the rostrolateral prefrontal cortex (RLPFC) and the cerebellum. The FPCN has been found to be active in a wide range of tasks involving cognitive control (for a meta-analysis see: Niendam et al., 2012) and has especially been linked to goal-directed cognition (Braver et al., 2009, Spreng et al., 2010b, Spreng et al., 2013, Vincent et al., 2008).

It has been suggested that older adults increasingly rely on the resolution of interference in later stages of processing (reactive control), to mitigate the effects of a reduced ability to prevent interference (proactive control, Braver, 2012, Braver et al., 2007). This is in line with a number of studies that have shown that (part of) the age-related impairment in selective attention stems from changes in perceptual stages of processing (de Fockert et al., 2009, Haring et al., 2013, Schmitz et al., 2010), which are likely to be related to reduced preparation for the upcoming stimulus (Geerligs et al., 2012b). However, so far it is not clear whether older adults can actually use additional reactive control mechanism in selective attention tasks to mitigate the effect of aging on proactive control. In the current study, we investigated whether there is evidence for increased use of reactive control mechanisms in older adults by increased recruitment of areas involved in the resolution of conflict, such as the FPCN or the anterior cingulate cortex (Carter and Van Veen, 2007).

Many studies examining the effects of aging on selective attention have either separated the relevant and irrelevant information in time, or spatially superimposed the relevant and irrelevant stimuli (e.g. de Fockert et al., 2009, Gazzaley et al., 2005, Gazzaley et al., 2008, Quigley et al., 2010). This is unlike situations often occurring in daily life, in which relevant and irrelevant information are typically spatially segregated. In the current study, we therefore use a selective attention task in which relevant and irrelevant information is presented simultaneously at different spatial locations. Participants are informed about the relevance of a location (i.e. one of the diagonals of a square) and about the letter identity of the “target” stimulus before each task block. The instruction is to identify a target stimulus among other stimuli, but only if it appears on a relevant location. This compares well to, for example, the real world situation of detecting a green light appearing in traffic lights. If the green light appears at another location, the ‘target’ needs to be ignored and is considered irrelevant.

In the selective attention task used here, participants responded by pressing a predefined button when the target appeared on a relevant spatial location. An alternative button was pressed if the target did not appear or if the target appeared on an irrelevant spatial location. Using the nontarget condition as a baseline, we were particularly interested in the effect of a target stimulus (detection effect) and the effect of an irrelevant target; that is, a target at an irrelevant spatial location (distraction cost), on response times, accuracy and neural measures. All three task conditions require adequate enhancement of relevant information as well as suppression of irrelevant information. However, by examining the change in response time between nontargets (i.e. no target letter presented) and irrelevant targets (i.e. target letter presented at an irrelevant diagonal position), we can infer to what extent the participant is able to suppress information presented on the irrelevant diagonal. If the participant is distracted by the irrelevant target, we would expect responses to be slower for irrelevant targets compared to nontargets. In the same way, comparing the nontarget condition to the target condition will provide information about how well participants are able to enhancing the processing of relevant stimulus features as well as relevant spatial locations. Using these different task conditions therefore, allowed us to study the effects of aging on reactive control during enhancement and suppression.

Based on the literature described above, as well as the results from our previous study using a highly similar task (Geerligs et al., 2012b), we expect that older adults will show increased distraction costs, particularly in response times. In the current study, we investigate the differences between age groups on reactive control mechanisms in selective attention, by comparing the neural signatures of the different task conditions. Early selection processes, that arise as a result of differences in proactive control, are expected to be the same over the different task conditions that contain highly similar visual stimuli. However, if older adults are able to use reactive control mechanisms to support selective attention, we would expect to find additional activation in brain areas involved in the resolution of conflict, such as the FPCN or the anterior cingulate cortex (Carter and Van Veen, 2007). This additional activation would be expected to be related to higher levels of performance in older adults. If no difference is detected in activation of these brain areas between age groups, this would suggest that older adults do not use more reactive control processes than young participants. Because selective attention requires the collaboration of different sets of brain regions, we investigated task dependent modulations in both activity and functional connectivity.

Section snippets

Participants

Forty younger (21 males, Mage = 20.6 years, age range: 18–26 years) and 40 older adults (24 males, Mage = 64.9 years, age range: 59–74 years) participated in the experiment. All participants were right handed and did not have a history of neurological or psychiatric disorders. They had normal or corrected-to-normal visual acuity. The older participants scored 26 or higher on the Mini Mental State Examination (MMSE, Folstein et al., 1975) and below 16 on both subscales of the Hospital Anxiety and

Behavioral data

In general, older participants had longer response times (M = 685, SD = 84) than younger participants (M = 523, SD = 70; F(1,68) = 81,80, p < 0.001). However, these effect of age group were modulated by task condition (task: F(2,126) = 57.89, p < 0.001; task*age group: F(2,126) = 27.02, p < 0.001). All participants responded faster to nontarget (NT) than to irrelevant target trials, although, this effect was larger for older than younger participants (age*IT–NT: F(1,63) = 18.02, p < 0.001; young: t(29) = 8.01, p < 0.001;

Discussion

The behavioral data are in agreement with previous research, suggesting that older adults show deficits in suppression of irrelevant information, while enhancement of relevant information is not affected by age (de Fockert et al., 2009, Gazzaley et al., 2005, Mager et al., 2007). Both age groups showed an increase in response times in irrelevant target compared to nontarget trials. This indicates that participants were not able to focus selectively on information on the relevant diagonal,

Acknowledgments

We would like to thank Marleen Eidhof, Christa Grosse-Schawe, Regina Vlasma and Enja Jung for their help in the data collection. In addition, we would like to thank Hedderik van Rijn for providing valuable discussions concerning the use of linear mixed effects models.

Disclosure statement

The authors declare no conflicts of interest.

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