We sought to determine whether having participants perform an auditory/phonological WM maintenance task concurrently with a visual WM task requiring selective attention would influence their ability to modulate activity in visual regions. Hypothesis-driven fMRI analyses focused on BOLD activation timecourses obtained from a scene-selective ROI, which was identified as the most robust marker of top-down modulation in a previous variant of this task (Gazzaley, Cooney, McEvoy, et al., 2005
). The digit WM load manipulation had no effect on visual WM-related activity in the scene-selective ROI during the Remember Scenes
or Passively View
conditions, but peak encoding activity in the Ignore Scenes
) condition was significantly elevated during high load trials relative to low load trials. This indicates that when taxed by high WM load, participants failed to appropriately attenuate processing of the irrelevant visual stimuli. The load-induced increase in distractor processing was further evidenced by the fact that participants showed better incidental long-term recognition memory, as assessed by a post-experiment recognition test, for irrelevant scenes they had previously encountered under high load than those that had appeared in low load trials.
Working memory resources and attentional control
The finding that irrelevant visual stimuli were excessively processed when participants had to concurrently maintain a high non-visual WM load suggests that distractor filtering, at least under these circumstances, requires active cognitive control. If attenuation of task-irrelevant scene representations in the Ignore Scenes
condition was merely a consequence of attentional resources being allocated to remembering faces, then activation of scene representations should have been further attenuated under high load by the additional attentional demands posed by digit maintenance. Thus, one can infer that the digit WM task usurps attentional control resources, presumably mediated by frontal and parietal lobe regions, that are involved in the maintenance and implementation of task goals and the associated top-down modulation of sensory processing (Bunge, Ochsner, Desmond, Glover, & Gabrieli, 2001
; Kane & Engle, 2002
; Mayer, et al., 2007
; McNab & Klingberg, 2008
). Our findings highlight the mechanistic overlap of WM and selective attention (Olivers, 2008
), and are generally consistent with the results of de Fockert and colleagues (2001)
, who also observed an increase in task-irrelevant visual processing when a WM load of four digits was imposed. In their study, famous face stimuli were always irrelevant, and participants had to judge whether the written name superimposed over each face referred to a politician or pop star. The profession associated with the names was often incongruous with that of the faces, creating Stroop-type conflict (Stroop, 1935
). Their results showed that fusiform activity, associated with face processing, increased under high WM load, but since the face stimuli were never task-relevant and they did not functionally localize a visual word form region, they were unable to draw conclusions about how the load manipulation influenced the enhancement of relevant visual information.
Our experimental approach offers the opportunity to expand upon these findings, given our ability to assess the consequences of non-visual WM load on both task-relevant and task-irrelevant visual processing, relative to a passive viewing control condition. Participants in our task were fully able to enhance the activation of relevant visual representations under high load, suggesting that increased WM load did not result in a generalized loss of modulatory control. Rather, the high load digit WM task selectively interfered with participants' ability to suppress or disengage their attention from task-irrelevant visual stimuli. Importantly, our results were obtained in a task setting in which there was no direct competition between relevant and irrelevant visual stimuli. Our stimuli were never simultaneously present, and thus did not compete directly for visuospatial attention and processing resources, nor were they structured to generate any Stroop-like semantic conflict with each other, unlike the stimuli and tasks used in previous studies (de Fockert, et al., 2001
; Egner & Hirsch, 2005
; Lavie, et al., 2004
). Our results thus suggest that the active cognitive control of distractor processing is not limited to situations in which explicit conflict between targets and distractors must be overcome.
Our findings are consistent with a number of behavioral studies investigating the role that WM resources play in inhibitory control. Performance on the antisaccade task is adversely affected by cognitive load, with participants making significantly more reflexive errors (looking towards the target when they should look away from it) when performing a concurrent mental arithmetic task (Roberts, Hager, & Heron, 1994
) or 2-back auditory letter WM task (Mitchell, Macrae, & Gilchrist, 2002
). Performance on the go/no-go task is also impaired by letter WM load (Hester & Garavan, 2005
). These studies suggest that WM resources are important for the suppression of prepotent responses. In the context of our task, control processes are likely needed to override the prepotent urge to attend to every picture. WM load manipulations have also been shown to influence negative priming effects, with the magnitude of negative priming, a putative index of inhibitory processing (Neill, 1977
), decreasing as verbal WM load increased (Conway, Tuholski, Shisler, & Engle, 1999
; Engle, et al., 1995
). Moreover, recent neuroimaging work utilizing within-subject conjunction analyses revealed that WM tasks and inhibitory control tasks often involve overlapping neural components (McNab, et al., 2008
Given that non-visual WM load selectivity impaired the regulation of task-irrelevant visual processing in our study while sparing control of task-relevant visual processing, it might seem that the high load digit WM task taxed cortical regions necessary for inhibitory control. However, we are hesitant to claim that the observed load effects reflect changing levels of top-down inhibitory signaling per se. Inspection of the raw activation timecourses () and their epoch-specific summaries () suggests that enhancement of task-relevant activity (Remember Scenes
> Passively View
) occurs earlier than the suppression of task-irrelevant activity (Passively View
> Ignore Scenes
). Interestingly, the load-dependent increase in task-irrelevant activity occurs during this earlier period (where the BOLD signal indexes initial image processing and encoding), with a similar temporal profile to that of the enhancement effect. Thus, the apparent WM load effect on distractor suppression may be alternatively conceptualized as inappropriate enhancement of task-irrelevant visual representations. This early over-activation of irrelevant representations on high load trials is counteracted later in the trial timecourse by successful suppression. During this later period, where BOLD signals presumably represent a mixture of residual stimulus processing activity and maintenance activity, the Ignore Scenes
activation level drops significantly below that of the Passively View
condition during both high and low load trials. This supports the view that modulatory attentional signals continue to exert their influence on the activation levels of specific posterior visual representations during WM maintenance (Lepsien & Nobre, 2007
; Lewis-Peacock & Postle, 2008
; Ranganath, Cohen, Dam, & D'Esposito, 2004
; Ranganath, DeGutis, & D'Esposito, 2004
). However, despite this late emergence of distractor suppression on high load trials, the early over-activation of irrelevant scene representations may be responsible for the stronger long-term memory representations formed for these scenes. This behavioral load effect is illustrated by the results of the surprise post-experiment recognition task (), in which participants reported no recognition of scenes they had encountered during low load Ignore Scenes
trials (i.e., they were rated as being no more familiar than novel scenes and significantly less familiar than scenes from Passively View
), while reporting a significantly stronger level of recognition for scenes encountered during high load Ignore Scenes
Our findings raise the question of why the high load digit WM task selectivity influenced the processing of task-irrelevant visual stimuli, while exhibiting little effect on the processing of task-relevant images. It is unlikely that the WM load manipulation caused participants to lose track of whether faces or scenes were relevant for a given trial, since trials from the three attentional conditions (Remember Faces, Remember Scenes, and Passively View) were blocked into separate scanning runs that lasted over six minutes each, giving participants ample opportunity to adopt a stable attentional set. Moreover, a generalized failure to maintain attentional processing priorities would have also resulted in diminished enhancement of relevant stimuli under high load. It is more plausible that the WM demands posed by the high load condition consumed critical attentional control resources necessary for implementing the efficient disengagement of one's attention from the irrelevant images. When performing the visual WM memory task blocks (i.e. not the Passively View condition) participants probably defaulted to a goal state in which they devoted a certain amount of attention to each image when it was first presented to maximize their opportunity to effectively encode it in the 800 ms allotted, should it be of the relevant stimulus class. In the low load condition, participants were readily able to prevent attention from being further allocated to images they determined to be irrelevant distractors, resulting in activation levels that peaked no higher than those obtained during passive viewing and subsequently dropped significantly below this baseline level. However, in the high load condition, the resource-demanding processes of assessing relevancy and/or terminating the perceptual analysis of distractors were likely delayed in their deployment. This resulted in an early over-processing of the irrelevant visual stimuli, whose neural representations were not successfully suppressed until later in the trial.
Had we designed this experiment with trial-unique attentional cues specifying whether faces or scenes were relevant, it is possible that the digit load manipulation would have resulted in a more general failure of task goal maintenance (Kane, Bleckley, Conway, & Engle, 2001
; Kane & Engle, 2003
), where the enhancement of relevant visual representations would also be compromised under high WM load. It is worth noting that our post-experiment recognition memory task did reveal a marginally significant decrement in the strength of long-term memory representations for those task-relevant scenes encountered under high load, relative to their low load counterpart. This suggests that at least a small cost of divided attention on the long-term encoding of relevant visual stimuli is present in our data, despite its failure to influence the degree of attentional enhancement observed in our scene-selective ROI.
However, given the disproportionate cost of WM load on distractor filtering, there may be something fundamentality different about the process of disengaging attention from distractors that makes this cognitive operation particularly vulnerable to fail when attentional control resources are depleted. Elegant behavioral work by Dosher and Lu (2000)
on the control of spatial attention has suggested that the process of filtering out irrelevant perceptual features (external-noise exclusion) is mechanistically separable from the process of enhancing the representations of relevant stimuli. The importance of a goal-directed distractor filtering mechanism is also suggested by recent neuroscientific work indicating that that the efficacy with which individuals can prevent task-irrelevant stimuli from being encoded into memory is a critical determinant of individual differences in WM capacity (McNab & Klingberg, 2008
; Vogel, et al., 2005
). The apparent dissociation between the enhancement of relevant stimuli and the filtering of irrelevant distractors may have more to do with the unique control processes that prevent the allocation of attention to distracting stimuli than the presence of a distinct top-down inhibitory (i.e. GABAergic) signaling system for suppressing irrelevant perceptual representations. Indeed, in a recent functional connectivity analysis exploring the strength of prefrontal interactions with a scene-selective ROI as a function of stimulus-relevance, we produced evidence suggesting that the successful filtering of irrelevant scene representations is mediated by a reduction in excitatory signals from the prefrontal cortex (Gazzaley, Rissman, et al., 2007
). However, excitatory and inhibitory signals are difficult to differentiate with BOLD fMRI, and thus the potentially important role of inhibitory signaling cannot be ruled out. While beyond the scope of the present manuscript, we hope that future work will help elucidate the complex interplay the between prefrontally-mediated goal representations and top-down modulatory control signals, so as to further our understanding of the neural mechanisms of distractor filtering.
Domain-general attentional control processes
The behavioral and neural effects that emerge when participants perform the high load digit WM task concurrently with the visual WM task suggest that these domain-specific WM tasks engage a common domain-general processing component. The digit sequences were presented auditorily to promote phonological encoding and maintenance, and yet the high load condition of this verbal WM task reduced the efficiency of visual selective attention and impaired visual WM performance. This cross-domain interference is consistent with the results of a recent behavioral study which found visual WM impairments when participants had to concurrently recite a random 7-digit sequence, but not when they had to recite their own telephone number (Morey & Cowan, 2004
). Such results indicate that visual and verbal WM maintenance likely rely on a common capacity-limited attentional control resource. Our results suggest that this shared processing resource is not only utilized to accommodate the attentional demands of high load maintenance, but is also involved in implementing the control necessary to attenuate the processing of distracting stimuli. However, we cannot rule out the possibility that at least some of the cross-domain behavioral interference observed under high load in our study is due to participants using verbal codes to support maintenance of the visual stimuli (Postle & Hamidi, 2007
), since participants' ability to form and rehearse verbal feature labels would likely be diminished on high digit load trials.
The existence of a domain-general attentional control resource does not preclude the existence of domain-specific attentional systems (Cocchini, Logie, Della Sala, MacPherson, & Baddeley, 2002
; Duncan, Martens, & Ward, 1997
), but rather suggests there are circumstances where these capacity-limited systems are not fully independent. Most demonstrations of WM load-dependent increases in distractor processing have involved verbal WM tasks performed concurrently with visual selective attention tasks. However, studies that have assessed the effect of visual WM load on the processing of visual distractors have found either no effect of WM load (Yi, et al., 2004
) or decreased distractor processing under high load (Rose, Schmid, Winzen, Sommer, & Buchel, 2004
). When visual attention is taxed by a perceptually demanding visual task, irrelevant visual distractors are typically strongly suppressed (Lavie, et al., 2004
; Pinsk, et al., 2004
; Schwartz, et al., 2005
; Yi, et al., 2004
). Limited within-modality attentional resources are easily exhausted by demanding perceptual tasks, which leaves little attention left over to process distractors, resulting in early and strong attentional gating (Lavie, 2005
). Thus, WM load manipulations will not always have the same consequences on distractor processing; the type of load is critical (Kim, Kim, & Chun, 2005
; Park, Kim, & Chun, 2007
). In our study, because the modality of the WM load did not overlap with that of the visual distractors, it did not facilitate their perceptual suppression. Rather, the auditory/phonological WM load likely interfered with amodal attentional control processes that are essential for regulating distractor processing.
Relationship of WM load effects to attentional deficits in cognitive aging
In the present study, we have demonstrated the selective effect of non-visual WM load on the ability of healthy young adults to attenuate the processing of task-irrelevant visual stimuli. It is interesting to note that a group of healthy older adults (60-77 years old) showed a strikingly similar failure to appropriately filter out distracting stimuli when they performed this same visual WM task without the additional burden of the digit maintenance task (Gazzaley, Cooney, Rissman, et al., 2005
). As with the present study's WM load manipulation, aging did not affect the enhancement of task-relevant representations. To illustrate the strong resemblance of this age-related suppression deficit to the present WM load effects, we extracted activation timecourses from the bilateral scene-selective ROIs of the 16 older adults from the Gazzaley et al. (2005)
. Much like younger adults under high WM load (), the activation pattern seen in older adults (, bottom) revealed an early over-activation of task-irrelevant representations. As expected, the younger control group from that study (, top) showed a pattern of enhancement and suppression effects similar to those observed in our study's low load condition. The weaker suppression effect observed in the low load condition of the present study (Ignore Scenes
activity did not drop significantly below the Passively View
baseline level until the portion of the timecourse indexing late encoding and maintenance activity) could be attributable to the fact that the low digit load still taxed WM resources to a certain extent. This may have served to reduce the degree of attainable suppression relative to that obtained in the Gazzaley et al. (2005)
study, which had no non-visual WM demands. It is noteworthy that both the effect of digit load and the effect of cognitive aging on distractor filtering were manifest early in the activation timecourse, and diminished during the maintenance period. While it is hard to make precise statements about cognitive timing based on fMRI data alone, a recent electroencephalogy (EEG) study using the same general task paradigm produced convergent evidence of an early over-activation of task-irrelevant representations in older adults, which interestingly was followed by successful suppression, as in the present study (Gazzaley, et al., 2008
). Thus, both cognitive load and cognitive aging appear to reduce the efficiency and/or speed with which distractor filtering operations can be brought to bear.
Fig. 6 Age-related impairment in suppression of task-irrelevant activity. Activation timecourses from a scene-selective ROI are plotted for groups of 17 younger adults and 16 older adults, who performed a version of the visual WM task used in the present study (more ...)
The fact that taxing young adults with a secondary WM task is sufficient to induce a similar top-down modulatory control deficit to that seen in the older population implies that older adults may have a reduced amodal WM capacity that is resulting in their selective suppression deficit. While simple WM maintenance tasks, such as digit span, are minimally affected by normal aging (Dobbs & Rule, 1989
), performance on complex WM span tasks, which assess the ability to use controlled attention in the face of interference, show age-related impairments (Gazzaley, Sheridan, Cooney, & D'Esposito, 2007
; Wingfield, Stine, Lahar, & Aberdeen, 1988
). Even though the digit WM task used in our study was a simple maintenance task, when performed in conjunction with a visual WM task that included distracting images, the same higher level domain-general WM resources depleted by aging were likely taxed. Future work will be needed to isolate the neuroanatomical substrates of capacity limitations in this critical controlled attention component of the WM system, especially given that individual differences in WM capacity are known to be highly correlated with individual differences in distractor filtering capabilities (Conway, Cowan, & Bunting, 2001
; Kane & Engle, 2003
; Vogel, et al., 2005
). While frontal regions have been implicated in both age-related cognitive impairments (Hedden & Gabrieli, 2004
; West, 1996
) and individual differences in WM capacity (Kane & Engle, 2002
), it remains to be seen whether the distractor filtering impairment observed in younger adults under high WM load is functionally homologous to those observed in older adults. To the extent that these goal-directed attentional control impairments are attributable to processing limitations in common brain structures, WM load manipulations, such as the dual-task approach used in the present study, may provide a useful tool for simulating and investigating both psychological and neurobiological aspects of cognitive aging.