During social interaction we often have to assimilate multiple pieces of incoming information in any given moment. To achieve this we use attention systems to filter relevant from irrelevant information, and working memory (WM) to monitor, update, and integrate ongoing current events. This enables us to forecast others’ intentions and plan one’s own behavior fluently and efficiently.

Social encounters are often rich with emotion. The presence of emotion during attention and WM tasks has been shown to strongly influence how we in turn perceive and process a situation, and there is evidence that particular emotions can both facilitate and impair performance, depending on the task at hand. Numerous studies report that attention is rapidly oriented and biased toward faces displaying fear or anger (Eastwood et al., 2003; Fenske and Eastwood, 2003; Fox and Damjanovic, 2006; Hahn et al., 2006; Horstmann et al., 2006; Bannerman et al., 2010; Feldmann-Wüstefeld et al., 2011; Huang et al., 2011) and toward threatening words and scenes (Fox et al., 2001; Yiend and Mathews, 2001; Koster et al., 2004). Within the normal human population this attentional threat bias is considered to be facilitatory in that it engages a primitive survival response to locate and process danger swiftly and effectively. There is also evidence that the presence of task-irrelevant threat can enhance the allocation of attention to a separate, unrelated task. For example, contrast discrimination is shown to be more sensitive when preceded by a fearful face (Phelps et al., 2006), and visual search efficiency for a prepotent target increases when preceded by a fearful face (Becker, 2009) or an emotional scene (Kristjánsson et al., 2012). Such knock-on effects of negative emotional stimuli on attention are widely considered to result from activation of amygdala and its associated networks (e.g., Phelps et al., 2006). In contrast, negative emotions have also been shown to impair rather than facilitate attention processes. Among anxious people, for whom the threat bias is particularly pronounced (e.g., Mogg and Bradley, 1998; Bradley et al., 2000; Fox et al., 2001), attention to threatening stimuli is associated with the inability to disengage from the threat item (Fox et al., 2001, 2002; Yiend and Mathews, 2001; Koster et al., 2004), a detrimental effect which may disrupt attention to other ongoing tasks. A disadvantageous bias to threat within the normal adult population is reported in a phenomenon called emotion-induced blindness, which describes impaired awareness of stimuli that follow in close temporal and spatial proximity to a negative emotional item (Most et al., 2005). A possible mechanism for these effects is that limited attention resources for high-level visual processing are directed toward irrelevant emotional stimuli and away from task relevant ones, thus impairing performance.

A smaller number of studies have asked whether emotionally positive stimuli have effects similar to those reported for negative stimuli. The general finding is that when stimuli are associated with reward and are therefore positive, they are highly effective at attracting attention. These effects have been found with a range of different stimuli including sexual stimuli (Arnell et al., 2007; van Hoof et al., 2010), drug related stimuli for addicted individuals (e.g., Bradley et al., 2004), and for arbitrary stimuli that have been associated with reward via conditioning (Raymond and O’Brien, 2009; Anderson et al., 2011). Other work suggests that arousal level of stimuli, positive or negative, determines their effect on attention (Anderson, 2005; Schimmack, 2005). Higher-level cognitive tasks are also affected by emotion, and again both facilitatory and detrimental effects of threat are reported. Complementing the advantageous threat bias in the attention literature, visual WM for the identity of faces is significantly better for faces bearing an angry (Jackson et al., 2009) or fearful (Sessa et al., 2010) expression than for faces bearing a positive or neutral expression. The ability to accurately maintain the identity of angry and fearful individuals in visual WM is likely to have evolved from the need to respond rapidly and appropriately to social threat cues. Note that the angry and happy faces used in our previous studies (and also used here) were rated very similar in arousal levels (see Jackson et al., 2009), therefore differences in arousal are unlikely to account for the finding of enhanced WM for angry faces.

Conversely, there are also disadvantageous effects of attention to negatively valenced information on separate, concurrent WM tasks. Task-irrelevant negative stimuli that are presented during a WM task have been shown to impair memory for neutral items, termed a distraction effect. For example, negative distracter words presented during the serial presentation of word memoranda impaired serial recall relative to positive and neutral words (Buchner et al., 2004). Similarly, Dolcos and McCarthy (2006) found that visual WM for neutral faces was significantly impaired when negative versus neutral or scrambled scenes were inserted as distracters into the WM maintenance period (see Dolcos et al., 2011, for a review of the neural correlates of such emotion-cognition interactions). These findings suggest that negative information although incidental detracts attention from an ongoing neutral task in which WM is engaged [see also the review by Cohen and Henik (2012) which outlines evidence that irrelevant emotional stimuli can both impair and enhance executive control].

What is unknown at present, however, is how task-irrelevant emotional information might impact upon a separate WM task when the memoranda themselves are emotional. Effective social engagement relies heavily on WM processes to maintain and update relevant person information, and this rarely occurs in an emotional vacuum. Facial expressions of emotion are crucial for rapidly communicating one’s own state of mind, and the ability to monitor others’ emotions over time is fundamental for normal human social interaction. With this in mind, in the current study we measured visual WM for angry and happy faces and assessed the impact of incidental negative, positive, and neutral words presented during a 9 s maintenance interval. We chose to use verbal rather than visual stimuli to act as intervening distracters because this study is a precursor to an fMRI investigation. This is the first use of emotional distracters in a WM task that also involves emotional items, therefore in using fMRI we want to be able to more clearly separate and examine brain activity in regions associated with the emotional faces (visual) compared to the emotional words (verbal).

Importantly, in the WM task two angry or happy faces were presented for encoding but the single test face presented at retrieval was always neutral. The task was to state whether the test person was present or absent at encoding and emotional expression was task-irrelevant. This design ensured that any effects of word valence on WM for emotional faces could be directly attributed to the presence of facial expression information at encoding and thus maintained during the retention interval, rather than a feed-forward effect of word valence on retrieval processes if facial expression were also present at retrieval (as was the case in the original studies that first reported the angry face benefit in WM; Jackson et al., 2008, 2009).

First, we assessed whether intervening words intended to distract from the WM task would interfere with memory for emotional faces at all. Dolcos and McCarthy (2006) found that neutral distracters impaired WM for neutral stimuli relative to a condition in which a scrambled distracter was presented, indicating that incidental non-emotional information, when meaningful, can interfere with WM maintenance processes. It is possible that emotional information held in WM is protected from such distraction in a way that neutral information is not, perhaps as a result of increased salience or enhanced motivational value. To test this, in Experiment 1 we directly compared the effect of intervening neutral words versus no words on WM for angry and happy faces. We favored a no-distraction condition over a scrambled word condition in order to provide a pure baseline measure of WM performance using a maintenance interval here (9000 ms) that is nine times longer than that used in the original studies of WM for emotional faces (1000 ms; Jackson et al., 2008, 2009). We used a particularly long delay interval because in the intended follow-up fMRI experiment we aim to measure brain activity during WM maintenance. Furthermore, comparing some versus no-distraction enhances the real-life validity of the test. To anticipate, we found no difference in WM performance between the two conditions for both angry and happy faces. On the one hand, it is possible that the absence of a distracter effect resulted from the relatively long maintenance interval and/or the neutral words used in the present study. On the other hand, this result also raises the interesting possibility that, when the contents of WM are emotional, some form of protection from distraction is afforded.

In Experiment 2, we again measured WM for angry and happy faces but this time directly compared the influence of negative, positive, and neutral intervening words. With this design we can predict several possible outcomes. If attention is biased to negative words, we would expect impaired WM for both angry and happy faces when negative versus both positive and neutral words are presented during WM maintenance, an effect that should result in a main effect of word valence. There is also reason to predict an interaction between word valence and facial expression on WM performance. Negative words might impair WM for happy faces to a greater degree than WM for angry faces (and vice versa: positive words might impair WM for angry faces to a greater degree that WM for happy faces) by virtue of incompatible valence interference. Alternatively, because WM has been found to be superior for angry versus happy faces (Jackson et al., 2008, 2009), suggesting enhanced maintenance of threat information, WM for angry faces in the current task might be protected from any distraction and remain unaffected by the valence of intervening words, while WM for happy faces might suffer from negative distraction. To anticipate, none of the above predictions were borne out, making our results both surprising and interesting. We found that emotional words (regardless of whether negative or positive) actually boosted WM for angry faces relative to the neutral word condition, whereas WM for happy faces was not significantly affected by word valence. The current study adds some interesting substance to the literature concerning the ability of emotion to enhance or impair cognition. Our findings call attention to the fact that information intended to distract from an ongoing task does not always serve to impair performance; incidental emotional material can facilitate WM when the memoranda signal threat.

In Experiment 1 we aimed to determine whether the presence of an intervening word had a distracting effect on WM for emotional faces relative to when no-distracter was present.

In Experiment 2 we aimed to determine whether WM for angry and happy faces was differentially affected by the valence of intervening words (negative, positive, neutral) presented during maintenance.

The current study reveals some interesting and perhaps unexpected effects of intervening emotional stimuli on WM for emotional faces. In contrast to previous research that showed impaired WM for neutral items when a negative versus neutral distracter is presented during maintenance (Dolcos and McCarthy, 2006), here we show that emotional versus neutral words presented during the maintenance period can boost WM performance, but only when items held in WM are negative in valence (angry faces). When items held in WM are positive (happy faces), there is little evidence that the emotionality of intervening words impacts on memory performance. However, a direct comparison of our findings with those of Dolcos and McCarthy (2006) is limited because we did not include a condition with neutral WM memoranda (see Caveats section at the end).

We also found that WM for expressive (angry or happy) face identities was not significantly affected by the presentation of neutral words during the retention interval relative to when the retention interval was devoid of new stimulation, a finding that raises the possibility that emotional content in WM may afford some form of protection from distraction. Future studies can verify this possibility by confirming that distracters impair WM for neutral faces, even when using a long maintenance interval and word distracters as in the present paradigm. Alternatively, it is possible that increased task difficulty afforded by the long retention interval served to modulate the distractibility of the words. Other work in this special issue shows that task difficulty can modulate the impact of emotional distracters (Jasinska et al., 2012).

There are two possible explanations for these effects. One possibility is that when angry faces are represented in WM, their emotional significance and valence leads to a state of heightened vigilance (over and above that afforded by happy face representations) for other potentially significant emotional events, a notion consistent with the theories regarding attention biases to threat stimuli (Öhman et al., 2001). Heightened vigilance could facilitate the ability of the emotional words to compete for selection to awareness, allowing them to elaborate the face representations already in WM and thereby improve performance in the task. Although WM for angry faces did not differ significantly between positive and negative word conditions, the elevation of WM for angry compared to happy faces was driven more by positive than negative words (Figure 3). If angry faces were already deemed threatening by virtue of their expression, then negative emotional words appearing during the retention interval would be less surprising, whereas positive words would present a contradiction that could have sparked greater elaborative thought and therefore better consolidation. It is also possible that our results are due to differences in arousal levels elicited by positive and negative words. For example, the theory of arousal-biased competition (ABC) proposes that arousal enhances memory for items that successfully compete for selective attention (Mather and Sutherland, 2011). Despite the fact that positive and negative words were rated as equally arousing when presented outside of the WM task (and that the angry and happy faces used here were rated as equally arousing; see Jackson et al., 2009), an ABC account might suggest that angry face representations maintained in WM received a greater arousal boost when a positive word appeared than when a negative word was presented (if attention were heightened by the contradiction in valence between the face and word). However, we can only speculate about such possibilities because the same cannot be said for happy faces followed by a negative word, and we did not measure attention to the word stimuli. It is possible that in this task (which depends on WM for face identity) the task-irrelevant expression information is discarded when the to-be-remembered faces are happy but retained when they are angry. Binding expression and identity may be more imperative with negative than positive expressions because the former more typically signal a need for an immediate change in action plans, whereas the latter do not. In this view, retaining the identity of happy faces may be unaffected by word valence simply because there is no emotional information being held in WM with which the word stimuli can interact. Other work in our lab, in which we probed the emotional contents of face WM by asking participants to categorize the valence of congruent or incongruently valenced stimuli during the retention interval, suggests that this indeed might be the case (unpublished data).

Of relevance to this explanation is another interesting aspect of our results, namely that the angry face benefit to WM found in our previous work using short (1000 ms) retention intervals (Jackson et al., 2008, 2009) is not observed when the retention interval is long (9000 ms) and either lacks additional stimulation or involves the presentation of neutral words (Experiment 1). During a longer WM retention interval there is greater scope for both visual face representations and the strength of associated emotional information to fade, and this might explain why we do not find the angry face benefit here. When, as in Experiment 2, another emotional event occurs during the longer retention interval, the fading angry memory trace may be reactivated and thus enable improved performance. However, it is important to note that there are other procedural differences between the current experiment and our previous work. Here, WM load was not varied and the probe face was always neutral, making the task more difficult.

Our main result was a facilitatory effect of incidental information (the emotional words) on WM performance for face identity. This facilitatory effect conforms to a growing body of literature showing that incidental information is not necessarily distracting, but can boost performance on a range of different tasks, including WM tasks. Several studies have now shown such effects with neutrally valenced but arousing (e.g., novel or otherwise salient) stimuli. SanMiguel et al. (2010) found that whether an unexpected sound led to impaired or improved WM for neutral faces depended on trial duration. They suggested that the orienting response induced by the unexpected sound can help to refocus attention in states of unfocused attention (longer trials) whereas it may distract from the task at hand in states of more focused attention (shorter trials). Similar facilitatory effects of novel sounds were found for a visual discrimination task by Wetzel et al. (2012). Using emotional stimuli as incidental distracters, Sutherland and Mather (2012) showed that negatively arousing sounds boosted WM for perceptually salient stimuli. Additionally, positive and negative visual scenes inserted into the WM maintenance period of a delayed discrimination task for letters have been shown to support memory performance while neutral distracter scenes impaired performance, relative to a no-distracter condition (Erk et al., 2007). Taken together these findings provide an emerging picture of how incidental emotional information can support rather than hinder online processing of other information.

The novel and important finding in our study is that the facilitatory effect of incidental emotional distracters on WM for face identity was confined to the condition involving social threat in the WM memoranda. Although we previously reported a benefit for angry faces in WM without the use of incidental distracters and with a brief retention interval (1000 ms; Jackson et al., 2008, 2009), here, using a long retention interval, we found this effect only when emotional words were presented during maintenance. This suggests that an additional “boost” from incidental emotional information is needed to support the advantage of threat-related information in WM over longer intervals. Other studies have shown that emotional (versus neutral) information presented during WM retention enhances activity in “hot” emotion areas and decreases activity in “cold” executive areas during a WM maintenance period (Dolcos and McCarthy, 2006; Wong et al., 2012). While such enhanced recruitment of emotion processing areas has been shown to impair WM for neutral items, it may conversely support the consolidation of emotionally salient information, such as threat cues, into WM.

In conclusion, we find facilitatory effects of incidental information with emotional content specifically on the retention of threat-related information in WM. Our previous work had shown that angry faces are particularly well retained in WM (Jackson et al., 2008, 2009), but the present results suggest that further WM consolidation over longer periods of time relies on an added boost of activation from emotion networks. Functional imaging work is required to directly assess the impact of these results on brain activity within hot emotion and cold executive regions.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.