Emotional stimuli capture spatial attention but do not modulate spatial memory

Vision Research 65 (2012) 12–20

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Emotional stimuli capture spatial attention but do not modulate spatial memory Rachel L. Bannerman ⇑, Elisha V. Temminck, Arash Sahraie Vision Research Laboratories, School of Psychology, University of Aberdeen, Aberdeen, Scotland, United Kingdom

a r t i c l e

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Article history: Received 18 October 2011 Received in revised form 22 May 2012 Available online 1 June 2012 Keywords: Attentional capture Saccadic localisation Spatial memory Corsi Blocks Task Emotion

a b s t r a c t There is evidence that emotional stimuli capture spatial attention and that visual memory is enhanced for emotional content. Here we examine the relationship between emotional content of stimuli and interactions with spatial memory. To assess spatial memory, a modified version of the Corsi Blocks Task (CBT), utilising emotional stimuli, was employed. In the CBT a series of spatial positions are highlighted and the participant has to repeat these in the order in which they were produced. Results showed that presenting more meaningful stimuli, such as emotional faces (e.g. angry or happy) at the spatial locations in the CBT did not enhance spatial memory span relative to the presentation of neutral stimuli (e.g. neutral faces) or non-image stimuli signified by a change in the luminance of the blocks. In addition, saccadic eye movements performed during retention disrupted spatial memory for all items. This occurred irrespective of whether the item to be remembered was a face, a luminance-defined stimulus or whether the face carried emotional significance. The results were not related to the visibility of the test stimuli as participants recognised the emotion displayed by the faces significantly above chance and rated emotional faces as being more arousing than neutral faces. Changes in the type of emotional stimulus (e.g. fearful faces, emotional schematic faces, spiders or flowers) or encoding (short vs. long) duration did not alter the pattern of results. These findings demonstrate an important dissociation between spatial capture and memory. Although emotional content can modulate orienting behaviour, it appears to be of limited effect on spatial memory. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction As humans, we have a limited capacity to process fully all of the perceptual information that reaches us at any one time. It has been argued that stimuli evaluated as emotionally meaningful, due to their adaptive value, have priority in this selection process, especially if they are associated with danger or threat (Öhman & Mineka, 2001). Several cognitive experimental tasks, including visual search, dot-probe and exogenous-cueing, have been utilised to investigate whether attention is drawn more rapidly towards the spatial location of emotional stimuli. In visual search tasks participants are required to search for a target stimulus amongst distracter stimuli. Using this task a number of studies have demonstrated that search times for negatively valenced face targets (e.g. angry) are faster than that for positive faces (e.g. happy) (Fox et al., 2000; Hansen & Hansen, 1988; Öhman, Lundqvist, & Esteves, 2001). This has been taken as evidence of a ‘threat-superiority effect’ which is thought to result from a predisposition to detect danger or threat rapidly

⇑ Corresponding author. Address: Vision and Attention Labs, School of Psychology, University of Aberdeen, Aberdeen, AB24 3FX Scotland, United Kingdom. Fax: +44 (0)1224 27342. E-mail address: [email protected] (R.L. Bannerman). 0042-6989/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.visres.2012.05.011

in our environment (Öhman, Flykt, & Esteves, 2001; Öhman, Lundqvist, & Esteves, 2001). Besides visual search, one of the best known methods of investigating preferential attention to emotion is attentional cueing. ‘Double’ and ‘single’ methods can be used, reflecting the number of cues. In the emotional modification of double cueing or ‘dotprobe’ tasks two images (usually an emotional and neutral face) are presented simultaneously for a fixed duration followed by the appearance of a dot-probe in one of the two image locations. Numerous studies have shown that anxious individuals responded especially fast when the probe replaced an angry face (Bradley et al., 1998; Bradley, Mogg, & Millar, 2000). Studies in the general population are few and results are mixed (see Bar-Haim et al. (2007) for review), but biases towards threat-related stimuli have been observed in normal individuals provided that specific stimuli (e.g. biologically relevant and/or highly threatening) or brief stimulus durations are used (Armony & Dolan, 2002; Cooper & Langton, 2006; Mogg et al., 2000). In single or ‘exogenous’ cueing, a cue (usually an emotional or neutral face) is presented in the left or right visual field followed by a target in the same (valid) or opposite (invalid) spatial location as the cue. Threat-related stimuli capture (e.g. faster for threat vs. neutral stimuli on valid trials) (Koster et al., 2006) and hold (e.g. slower for threat vs. neutral stimuli on invalid trials) (Fox, Russo, Bowles, & Dutton, 2001) attention in anxious individuals. This

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pattern is also observed in the normal population provided that specific stimuli and methodological criteria are met (see Bannerman, Milders, & Sahraie, 2010a, 2010b; Koster et al., 2004, 2007; Phelps, Ling, & Carrasco, 2006). Given the myriad evidence suggesting that emotional stimuli capture our attention, an interesting question arises on how memory for spatial location would be affected by emotion. Research which has investigated the impact that emotional stimuli have on memory has mainly focused upon visual (as opposed to spatial) memory and has differentiated two types of visual memory; The ability to maintain information over short delays (e.g. a few seconds) (Short-Term-Memory: STM) or long delays (e.g. hours, days and even decades) (Long-Term-Memory: LTM). It is well established that visual LTM is enhanced for emotional images and that this effect is especially strong when the emotional image is negative (Dolan, 2002; Kensinger, 2007; La Bar, 2007). Several explanations for this visual LTM emotional memory advantage have been proposed. These include enhanced attention to emotional content at encoding (Schupp et al., 2003), greater elaboration on autobiographical or semantic features of emotional stimuli (Christianson & Engelberg, 1999; Doerksen & Shimamura, 2001; Phelps, LaBar, & Spencer, 1997), increased rehearsal of emotional information (Christianson & Engelberg, 1999) and greater distinctiveness and uniqueness of emotional (vs. neutral) stimuli (Christianson & Engelberg, 1999; Pesta, Murphy, & Sanders, 2001) all contributing towards beneficial long-term retention of emotional information. While these processes would also be expected to influence visual STM, it is worth noting that results for visual STM are more varied. There is some evidence that visual STM for face identity is enhanced when the faces display angry expressions compared to neutral or happy expressions (Jackson et al., 2008, 2009). However, it has also been shown that the valence of faces, pictures or words does not modulate visual STM (Kensinger & Corkin, 2003). Part of the explanation for enhanced visual LTM for emotional information but discrepant visual STM findings may relate to consolidation processes (Cahill & McGaugh, 1998). Emotional information is likely to be more frequently consolidated than neutral information. Indeed emotional enhancement in memory has been shown to increase as the retention interval increases (Cahill et al., 1996; Canli et al., 1999, 2000; Tabert et al., 2001). Another explanation concerns retrieval processes. As discussed by Kensinger and Corkin (2003) emotion may act as a cue at retrieval, potentially making retrieval of emotional information easier than neutral information because of the additional contextual support. Limited research has investigated whether emotion also enhances spatial memory. Of the few studies examining emotion and spatial memory, all have focussed upon emotional state. For example, there is evidence that depressed individuals (Miller et al., 1995) or those reporting high levels of negative affect (Tucker et al., 1999) have impairments in spatial localisation tasks. Other studies have examined the relationship between cortisol, thought to be increased in depressive disorders (Schulkin, Gold, & McEwen, 1998), and spatial memory performance, often with inconsistent findings. For example, individuals with heightened levels of cortisol, either basally or through acute administration, are better at relocating a series faces to their original location in a large matrix when the faces display negative emotions (e.g. anger) (Putman, Hermans, & van Honk, 2007) or are poorer at relocating happy faces (Van Honk et al., 2003). However, evidence for an inverse relationship between cortisol and spatial memory of anger has been documented whereby participants with higher levels of cortisol display poorer performance on memory of the locations of angry faces (Van Honk et al., 2003). Alternatively, in another study cortisol had no effect on short-term spatial memory (Putman et al., 2004). The question of whether emotion can modulate

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spatial memory when the emotional content of the stimuli is manipulated, rather than the emotional state of the participant, remains to be answered. It would certainly be advantageous to remember the location where a danger/threat was presented in the environment, but how might emotion modulate spatial memory? A possible mechanism could involve attention, often thought of as the gatekeeper for STM (Bundesen, 1990; Duncan & Humphreys, 1989). Emotional faces, especially anger or fear, appear to be particularly good at capturing attention (Bannerman et al., 2009; Bannerman, Milders, & Sahraie, 2009, 2010a; Hansen & Hansen, 1988; Öhman, Flykt, & Esteves, 2001; Öhman, Lundqvist, & Esteves, 2001), even when they are task-irrelevant (Eastwood, Smilek, & Merikle, 2003), thus attention could first be drawn more effectively to the spatial location of such faces and emotion may therefore influence spatial memory through the mechanism of attention. There are several lines of evidence to suggest a link between attention and spatial span. Firstly, it has been proposed that spatial attention is involved in maintaining spatial items in order in memory in that spatial memory is disrupted by any task which also makes demands on spatial attention (Smyth & Scholey, 1994). Secondly, multiple object tracking, which involves maintaining the spatial location of several target items as they move about randomly amongst distracters for several seconds, is affected by attention. Notably, ERP components reflecting the effect of attention reduce in amplitude with increasing attentional load (Sternshein, Agam, & Sekuler, 2011). Thirdly, evidence also suggests a correlation between brain circuits that mediate spatial attention and spatial memory in that both are driven by a right hemisphere dominant network of frontal and parietal sites (Awh & Jonides, 1998; Awh, Smith, & Jonides, 1995; Chelazzi & Corbetta, 2000). This anatomical overlap suggests a functional relationship between spatial capture and spatial memory (Awh & Jonides, 2001). This is corroborated by evidence which shows that storing an object in STM, facilitates attentional capture by that object (Downing, 2000; Pashler & Shiu, 1999) and that increased attention to spatial context increases spatial memory (Kentros et al., 2004). Thus enhanced attention to emotional information could modulate spatial memory due to the functional relationship between the spatial attention and memory systems. Emotional faces might subsequently be encoded more efficiently than neutral faces because emotion has been found to facilitate sensory processing (Schupp et al., 2003). Emotion has also been suggested to facilitate the consolidation and maintenance processes of visual STM, with enhanced visual STM for emotional face identities, especially angry (Jackson et al., 2009). Applying this notion to the spatial domain, it is possible that there is a relative benefit for maintained spatial location when the location is cued by an emotional vs. a neutral face. However, it is important to consider that rather than benefit, emotion might hinder or have no effect on spatial memory. For example, aside from capturing attention, emotional stimuli can hold attention and are particularly difficult to disengage from (Bannerman, Milders, & Sahraie, 2010a, 2010b; Fox et al., 2001; Koster et al., 2004, 2006, 2007). This focused processing on emotional content may be at the expense of task performance. Research has also suggested separate stores for visual and spatial information. For example, behavioural studies have differentiated between visual and spatial memory, with spatial memory tasks being disrupted more by spatial interference than visual interference, while the reverse pattern is shown for visual memory tasks (Della Sala et al., 1999). There is also neuropsychological evidence of patients who have deficits in spatial, but not visual STM, or the opposite pattern (Della Sala & Logie, 2002). Furthermore, neuroimaging studies have shown regional variations in the human prefrontal cortex as a function of visual vs. spatial memory loads

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(Baker et al., 1996; Courtney et al., 1996; McCarthy et al., 1996; Owen et al., 1998; Smith et al., 1995). This distinction is thought to rely on visual and spatial codes which are linked to separate visual processing pathways that are thought to encode ‘what’ and ‘where’ information respectively (Smith et al., 1995). Therefore, given this dissociation, it is possible that having emotion as visual cues may not modulate spatial memory. That said, it is important to note that evidence for separate visual and spatial stores remains controversial. A review of neuroimaging data has suggested that results from neuroimaging investigations of visual and spatial dissociations are inconclusive (Nystrom et al., 2000) and several limitations (including a static vs. dynamic distinction as opposed to a visual vs. spatial) have been directed at the behavioural data (Pickering et al., 2001; Postle & D’Esposito, 2000; but see Klauer & Zhao, 2004). Therefore, the goal of the present study was to examine whether emotional content affects spatial memory. It remains unclear whether emotional information benefits, hinders or has no influence on spatial memory. We investigated this issue using a modified version of the Corsi Blocks Task (CBT: Corsi, 1972). Originally designed to measure spatial short-term memory in neurological patients (Milner, 1971), the CBT consists of a set of nine wooden blocks arranged randomly on a board which are touched in sequence by the experimenter. The participant is required to reproduce the sequence in order, and his/her spatial memory span is defined as the number of items they can reproduce, without making a recall error. No research has examined whether spatial memory span, in the CBT in particular, is affected by characteristics of to be remembered spatial sequences. Notably, it is not clear how the meaning (or emotional content) of to be remembered spatial stimuli influences spatial memory span. Previous studies on spatial working memory have also shown that short-term memory of spatial location can be disrupted by several secondary tasks, including saccadic eye movements (Baddeley, 1986; Hale et al., 1996; Lawrence, Myerson, & Abrams, 2004; Lawrence, Myerson, Oonk, & Abrams, 2001; Pearson & Sahraie, 2003; Postle et al., 2006), limb movements (Logie & Marchetti, 1991; Pearson, Logie, & Gilhooly, 1999; Quinn, 1991; Quinn & Ralston, 1986; Smyth, Pearson, & Pendleton, 1988; Smyth & Pendleton, 1989) and shifts of spatial attention that occur in the absence of saccadic eye or limb movements (Smyth, 1996). Furthermore, the extent of interference caused by saccadic eye movements is greater than that caused by limb movements or a shift of attention with the eyes fixated (Lawrence, Myerson, & Abrams, 2004; Pearson & Sahraie, 2003), suggesting that saccadic eye movements can act as a unique form of disrupter in temporary memory for spatial location. Greater disruption of spatial memory by consecutive irrelevant saccadic eye movements has been proposed to reflect a mechanism that relies on properties specific to eye movements (e.g. their visual consequences such as production of visual transients, saccadic suppression and changes in retinal co-ordinates) (Lawrence, Myerson, & Abrams, 2004). Interference in an oculomotor control network, including the frontal eye fields and the superior colliculus, has been proposed (Pearson & Sahraie, 2003). However, it is also not known how the magnitude of interference (particularly by saccadic eye movements) is influenced by the emotional content of to be remembered spatial stimuli. Enhanced attentional capture by emotional stimuli and/or more efficient encoding/consolidation of these items in memory might lead to emotion overriding any disrupting effects of saccades. We know that emotional stimuli are, to a certain extent, able to resist other visual phenomena such as the attentional blink (de Jong et al., 2009; Maratos, Mogg, & Bradley, 2008; Milders et al., 2006) and the saccadic disruption effect of spatial memory may be another example of a phenomenon which is not fallible to emotion. Alternatively, saccadic eye movements may disrupt spatial memory for all stimuli, irrespective of

emotional meaning. This may arise from interference in an oculomotor control network including the superior colliculus in particular. The superior colliculus, along with the pulvinar in the thalamus, is involved in emotion processing via links with the amygdala (Anderson & Phelps, 2001; Le Doux, 1996). Linked to memory, activation of the amygdala may modulate hippocampal function, which may subsequently modulate consolidation processes (Cahill, 1999; McGaugh, 2000; McGaugh, Cahill, & Roozendall, 1996). If saccadic eye movements interfere with superior colliculus processing this may disrupt subsequent amygdala and hippocampal function and result in a spatial memory cost for all stimuli, including emotional. Therefore, the goal of the current study was to determine the impact that emotional stimuli have on spatial memory. In Experiment 1 it was examined whether presenting more meaningful stimuli, such as emotional faces at the spatial locations in the CBT would enhance spatial memory span. In addition, it was explored whether saccadic eye movements performed during retention also disrupt spatial memory of these more meaningful stimuli, or whether the emotional and adaptive value of such stimuli enables them to negate such a reduction. Five further controls addressed the possible influence on our results of recognition/ arousal of face stimuli, encoding duration of each face, choice of negative emotion (e.g. fear vs. anger), and type of emotional stimulus (e.g. real faces, schematic faces, or emotional pictures such as spiders and flowers). 2. Experiment 1 2.1. Methods 2.1.1. Participants Twenty participants (17 female, 3 male; mean age = 24.9 years; range 20–38) took part. All had normal or corrected to normal vision and normal state (M = 32.7; SD = 8) and trait (M = 34.8; SD = 7) anxiety levels as measured by the State-Trait Anxiety Inventory (STAI; Spielberger, Gorsuch, Lushene, Vagg, & Jacobs, 1983). The experiment was approved by the University of Aberdeen ethics committee and performed in accordance with the ethical standards laid down in the Declaration of Helsinki. All participants gave informed consent. 2.1.2. Stimuli and procedure Participants’ spatial memory span was measured using an irregular array of nine blocks based on the CBT (De Renzi & Nichelli, 1975), and modified for display on a PC monitor. The Corsi blocks display (35 cm  26.5 cm; 43.4°  35.6°) was presented centrally against a uniform grey background (26 cd/m2). Each block, subtended 4.5 cm  4.5 cm (6.9°  6.9°). Face stimuli consisted of greyscale pictures of nine female individuals; each displaying an angry, happy or neutral expression, taken from the Karolinska Directed Emotional Faces set (KDEF: Lundqvist, Flykt, & Öhman, 1998). Faces were sized to fill the entire block and consequently also subtended 6.9°  6.9°. Participants viewed the display at a viewing distance of 37 cm with their head position stabilised. In each trial (see Fig. 1 for trial sequence) the array of blocks appeared on the screen, and participants fixated a central cross. A series of transient visual events then occurred denoted by (a) a momentary change in luminance of a block from grey (26 cd/m2) to black (0.65 cd/m2) for 250 ms followed by return to the background luminance for 250 ms in the baseline condition or a momentary change to (b) an angry (c) a happy or (d) a neutral face stimulus appearing inside a block for 250 ms in the angry, happy and neutral face conditions, respectively. Baseline, angry, happy and neutral conditions were blocked. Corsi block selection was carried out randomly with the restriction that no block was selected

R.L. Bannerman et al. / Vision Research 65 (2012) 12–20

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Fig. 1. Schematic representation of presentation sequence in CBT Experiments. Events run in the direction top left to bottom right and represent (1) initial presentation of the array of blocks (1000 ms), (2) presentation of the events indicated by a transient change in luminance of a block (baseline condition) or a change to a face stimulus (angry, happy or neutral) appearing inside the blocks for 250 ms followed by a 250 ms interstimulus interval before the presentation of second event (also for 250 ms), (3) 5-s retention interval with presentation of uniform field with fixation point (pictured) or saccadic tracking task and (4) blocks reappear and participants indicate the position and order of events using the mouse cursor.

twice in each trial. At the end of the sequence the blocks disappeared signalling the start of a 5-s retention interval. During the retention interval participants were instructed to maintain fixation on a central fixation point or in the saccadic eye movement task, to track a dot that appeared alternating in position between the left and right side of the screen. The dot appeared in the same position as the fixation point at the beginning of the retention interval and then appeared either side of the screen (22.7° from the centre) at 0.8 Hz frequency. Participants were instructed to keep their eyes focused on the dot throughout the retention interval. Although the saccade task took more effort than the fixation task, previous research has shown that the extent of interference in spatial memory caused by saccades is greater than that caused by other secondary tasks (e.g. limb movements, smooth pursuit eye movements) also involving expending effort (Lawrence, Myerson, & Abrams, 2004; Pearson & Sahraie, 2003). This suggests that any disruption due to saccades cannot simply be explained by the greater effort expended. At the end of the retention interval the blocks reappeared and participants recalled the sequence of presented events by pointing and clicking the mouse curser on previously highlighted blocks in an identical order to that of presentation. Participants were free to move their eyes during the recall of the sequence and were given an unlimited amount of time to make their responses. Each participant performed four conditions (baseline, angry, happy and neutral) with two retention tasks (eyes fixated and saccadic eye movement) at each condition. To ensure compliance with the experimental instructions, horizontal and vertical eye movements were recorded using electrooculography (EOG). Resulting EOG signals were monitored online by the experimenter to check that participants either maintained fixation or moved their eyes when required. Failure to comply with the instructions would result in the trial being re-run. Across all experiments, compliance with the experimental instructions was excellent and no trials were omitted or re-run. To ensure accurate and consistent measurement, spatial span was calculated using a staircase procedure (see Hulme, Maughan, & Brown, 1991; Logie et al., 1996; Logie & Pearson, 1997; Pearson & Sahraie, 2003). Participants first completed a series of practice

trials and then proceeded to the experimental trials. Participants performed one experimental run for each of the eight different conditions (baseline, angry, happy and neutral with eyes fixated retention task) and (baseline, angry, happy and neutral with saccadic eye movement retention task). Pilot testing (n = 5) revealed no significant differences in spatial span when participants performed one experimental run per condition compared to multiple (five) runs. This was true for baseline (M = 4.19 vs. 4.26), angry (M = 4.80 vs. 4.60), happy (M = 4.67 vs. 4.13) and neutral (M = 4.19 vs. 4.47) conditions in the eyes fixated retention task (all p’s > .2) and baseline (M = 2.33 vs. 2.47), angry (M = 2.93 vs. 2.73), happy (M = 2.93 vs. 2.93) and neutral (M = 2.30 vs. 3.00) conditions in the saccadic eye movement retention task (all p’s > .3). Therefore it was deemed sufficient to limit testing to one run per condition. For each experimental run, trials were grouped in blocks of three. In the first block only two sequential transient events were presented per trial. Following the retention interval the participant reported the position and order of the visual events. If at least two out of the three trials were correctly identified then an additional block was presented. The number of transient visual events was increased sequentially in the consecutive blocks (i.e. 3 events, 4 events, 5 events . . . up to a maximum of 9 events), and the experimental run was terminated if more than two trials were reported incorrectly in any one block. Therefore, consistent with previous research (Pearson & Sahraie, 2003), the maximum load/sequence length was determined on an individual basis. The spatial span was calculated as the average number of events in the last three correct trials. 2.2. Results Mean spans in each condition are displayed in Fig.2. Mean spans were analysed using a 4 condition (baseline, angry, happy and neutral)  2 retention task (eyes fixated and saccadic eye movement) within-subjects ANOVA. This revealed a significant main effect of retention task, F(1, 19) = 27.53, p < .001, g2p ¼ :59. Saccadic eye movements performed during the retention interval significantly disrupted spatial span (M = 3.32; SD = .97) relative to fixation only

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Fig. 2. Mean Spatial Spans for baseline, angry, happy and neutral conditions in fixation only (dark grey bars) and saccadic eye movement (light grey bars) task in Experiment 1. Error bars represent standard errors of the mean (SEM).

(M = 4.67; SD = .72). Demonstrating the strength of this main effect, a series of paired samples t tests showed that saccadic eye movements disrupted spatial memory in all conditions; baseline, angry, happy and neutral (all p’s < 0.01). There was no main effect of condition, F(3, 57) = 1.92, p = .137, g2p ¼ :09, and no condition x retention task interaction, F(3, 57) = 1.47, p = .233, g2p ¼ :07. Therefore, Experiment 1 has shown that spatial span in the CBT is not modulated by emotional content and that saccadic eye movements disrupt spatial memory for all items. This occurs irrespective of whether the item is a face or non-face stimulus or whether the face carries emotional significance. To ensure that the observed absence of emotional modulation in spatial memory was a robust effect and not simply related to task/stimuli issues we conducted several manipulations reported below.

2.2.1. Additional experimental manipulations Firstly, as the face stimuli were presented for a short duration (250 ms), it is possible that the emotional expression was simply not seen. We examined this issue by getting a subset of participants to perform a recognition task in which they were required to identify the emotional expression of each face (choosing from seven possible options: anger, fear, happy, sad, surprise, disgust or neutral) as it appeared for 250 ms in the CBT display. Arousal ratings for each face were also recorded. Participants were able to recognise the emotion displayed on the face in the CBT display significantly above chance (angry M = 71.8%; SD = 28, happy M = 86.7%; SD = 14, neutral M = 79.2%; SD = 18: all p’s < .05), and rated emotional faces (angry M = 3.63; SD = .70, happy M = 4.08; SD = .42) as significantly more arousing than neutral faces (M = 1.53; SD = .73) (both p’s < .001), suggesting that emotion was visible to participants. Secondly, we assessed whether using schematic faces which are widely used in emotion research (see Bannerman, Milders, & Sahraie, 2009) to remove feature ambiguity and to simplify the facial stimuli would lead to emotional enhancement. Thirdly, given the peripheral presentation of faces, we examined whether utilising fearful faces (as opposed to angry faces) which convey a peripheral advantage in detection tasks (Bannerman, Milders, & Sahraie, 2009; Bannerman, Milders, & Sahraie, 2010a, 2010b; Bayle, Henaff, & Krolak-Slamon, 2009) would enhance spatial memory span. Fourthly, given that performance on the CBT has been found to improve with longer encoding intervals (Fischer, 2001) we examined whether increasing stimulus duration to 500 ms, thereby lengthening the encoding time of each face would lead to emotional modulation in the CBT. The use of schematic faces, fearful faces

and longer stimulus durations did not affect spatial memory span (see Table 1). However, it has been proposed that in order for emotional-bias to be observed in non-anxious individuals, the stimuli need to exceed a certain threshold value (i.e. the stimuli must be highly threatening and/or pose a genuine threat value) (Armony & Dolan, 2002; Koster et al., 2004, 2007). Therefore, it is possible that the face stimuli employed did not meet these criteria. Consequently we also examined whether using emotional stimuli where location actually matters (e.g. spiders) may enhance memory span. Fear of spiders is common and remembering the location of such stimuli would be adaptive because of their potentially dangerous nature (e.g. being bitten and killed) (Fredrikson et al., 1996; Öhman & Mineka, 2001). Indeed in visual search tasks spiders are detected more quickly amongst positive (e.g. flowers) and neutral (e.g. mushrooms) distracters than flowers or mushrooms are amongst spiders (Öhman, Flykt, & Esteves, 2001). Moreover, our arousal data showed that images of spiders were rated as more arousing (M = 4.13; SD = .63) than images of angry faces (real: M = 3.63; SD = .70, schematic: M = 3.85; SD = .57). Therefore, we presented emotional stimuli with genuine threat value (e.g. spiders), positive images (e.g. flowers) and neutral images (e.g. mushrooms) at the spatial locations in the CBT. Presentation of these stimuli did not lead to any emotional modulations in spatial memory span (see Table 1). In sum Experiment 1 and the various manipulations conducted revealed a consistent pattern of results. Presentation of emotional stimuli does not enhance spatial memory span and cannot overcome previous deficits observed with saccadic movements. This pattern stands despite changes in stimulus duration (250 ms or 500 ms) or type of emotional stimulus (angry/happy/fearful faces or spiders/flowers). Given that the experimental design of Experiment 1 and the additional manipulations was essentially identical this allowed us to conduct analyses on the combined data (total N = 100) in order to examine whether the null effect of emotion was related to power issues. 2.2.2. Analyses on combined data from Experiment 1 and the additional manipulations Given that there were no significant differences in the pattern of results obtained using fearful or angry faces or images of spiders, for the purpose of the combined analysis we collapsed across these images to form a ‘negative image category’. Likewise data from happy faces and flower images formed a ‘positive image category’ and data from neutral faces and mushroom images formed a ‘neutral image category.’ Analyses on the combined data revealed a significant main effect of retention task, F(1, 99) = 176.52, p < .001, g2p ¼ :64, resulting from saccadic eye movements performed during retention significantly disrupting spatial span (M = 3.57; SD = .99) relative to fixation only (M = 4.75; SD = .82). Paired samples t tests showed that saccadic eye movements disrupted spatial memory in all conditions; baseline, negative, positive and neutral (all p’s < 0.001). The combined analysis also revealed a significant main effect of condition, F(3, 297) = 2.88, p < .05, g2p ¼ :03, although Bonferroni pairwise comparisons revealed that this effect was driven by enhanced spatial span in the neutral condition (M = 4.28; SD = .99) relative to the baseline condition (M = 4.03; SD = .95) (p < 0.05). No other comparisons were significant (all p’s > .4). The condition x retention task interaction was also significant, F(3, 297) = 3.49, p < .05, g2p ¼ :03. To interpret this interaction, separate ANOVA’s were conducted for each retention task. For fixation only, the main effect of condition was not significant, F(3, 297) = 1.06, p = .369, g2p ¼ :01. Therefore the type of stimulus (e.g. luminance defined block, negative, positive or neutral image) did not modulate spatial memory span in the fixation only task. For saccadic eye movements, the main effect of condition was

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Table 1 Results of additional experimental manipulations. The use of schematic faces, fearful faces, longer stimulus durations and spider/flower stimuli did not lead to emotional modulation in spatial memory span. Manipulation

Angry, happy and neutral schematic faces (250 ms)

Fearful, angry, happy and neutral real faces (250 ms)

Fearful, happy and neutral real faces (500 ms)

Spiders, flowers and mushrooms (250 ms)

Participants

N = 20 (14 female, 6 male; mean age = 25.5 years)

N = 20 (14 female, 6 male; mean age = 24.1 years)

N = 20 (6 female, 14 male; mean age = 28 years)

N = 20 (6 female, 14 male; mean age = 28 years)

Mean (SD)

Mean (SD)

Fixation only spatial span

Saccadic eye movement spatial span

Baseline: 4.38 (1.01)

Baseline: 3.20 (1.27)

Angry: 4.08 (1.00) Happy: 4.30 (1.03) Neutral: 4.62 (1.01)

Angry: 3.52 (1.12) Happy: 3.28 (1.62) Neutral: 3.40 (1.20)

Baseline: 4.85 (1.03)

Baseline: 3.02 (1.55)

Fearful: 4.55 (.67) Angry: 4.75 (.82) Happy: 4.82 (.91) Neutral: 4.75 (.81)

Fearful: 3.37 (.70) Angry: 3.88 (1.29) Happy: 3.76 (1.28) Neutral: 3.66 (1.41)

Baseline: 4.98 (1.12)

Baseline: 3.81 (.99)

Fearful: 5.10 (1.06) Happy: 5.03 (1.04) Neutral: 5.15 (.93)

Fearful: 4.15 (1.26) Happy: 3.78 (1.11) Neutral: 4.15 (1.13)

Baseline: 5.03 (.96)

Baseline: 3.67 (1.19)

Spiders: 4.82 (1.42) Flowers: 4.73 (1.01) Mushrooms: 4.97 (1.12)

Spiders: 3.78 (1.43) Flowers: 3.68 (1.37) Mushrooms: 3.97 (1.67)

significant, F(3, 297) = 4.15, p < .01, g2p ¼ :04. Bonferroni pairwise comparisons revealed significant differences in spatial span between the baseline (M = 3.31; SD = 1.35) vs. neutral (M = 3.75; SD = 1.35) and baseline vs. negative (M = 3.72; SD = 1.17) conditions (both p’s < 0.05). No other comparisons were significant (all p’s > .4). In summary, the combined analysis has shown that consistent with the individual analyses of each experiment, presentation of emotional stimuli does not enhance spatial memory span in the CBT in conditions where participants remain fixated during the retention interval. In conditions where participants are required to make saccadic eye movements the combined analysis showed the type of stimulus can affect spatial span with increased span when a negative or neutral stimulus is presented relative to a simple luminance defined block. That said, there were no differences between emotions (e.g. negative/positive vs. neutral or negative vs. positive). In addition, saccadic eye movements disrupted spatial memory span in every condition (baseline, negative, positive and neutral), suggesting that the emotional meaning of the stimuli could not negate the saccadic deficit.

3. General discussion The current study investigated whether spatial memory span in the CBT was modulated by the emotional content of to be remembered spatial stimuli and whether saccadic eye movements performed during retention also disrupted temporary maintenance of location of these meaningful stimuli. Across experiments a consistent pattern of results was found whereby spatial span was not modulated by emotion. Angry, fearful and happy faces did not benefit spatial span relative to neutral faces or the baseline condition where block selection was highlighted by a simple luminance change. Likewise, spiders and flowers did not enhance spatial span relative to mushrooms or simple luminance defined blocks. Moreover, saccadic eye movements disrupted spatial memory for all items. This occurred irrespective of whether the item to be remembered was a face, a picture or a luminance defined stimulus or whether the face/picture carried emotional significance.

Condition

Retention task

Condition  retention task

p = .639

p < .001

p = .361

p = .144

p < .001

p = .125

p = .326

p < .001

p = .797

p = .613

p < .001

p = .629

The absence of emotional modulation could not be explained simply by emotion not being visible to participants as participants recognised the emotion displayed by the faces significantly above chance and rated emotional faces as being more arousing than neutral faces when they were presented for 250 ms. Increasing the stimulus duration to 500 ms, consequently doubling the encoding time of each face, made little difference to the pattern of results obtained. Emotional faces still did not enhance spatial memory span, nor did they overcome the past saccadic deficit. The null effect of emotion was also not due to a lack of power as analysis on the combined data (total N = 100) revealed that emotional images did not benefit spatial memory span during fixation conditions of the CBT and that saccadic eye movements resulted in a drop in spatial span across all image conditions (baseline, negative, positive and neutral). Despite emotion having no effect on spatial memory span in the current study, previous studies have shown that emotional stimuli capture spatial attention more effectively than neutral stimuli (Bannerman, Milders, & Sahraie, 2010a, 2010b; Fox et al., 2000, 2001; Hansen & Hansen, 1988; Koster et al., 2004, 2007; Mogg et al., 2000; Öhman, Flykt, & Esteves, 2001; Öhman, Lundqvist, & Esteves, 2001). Given the functional overlap between spatial attention and memory systems (Awh & Jonides, 1998, 2001; Awh, Smith, & Jonides, 1995; Chelazzi & Corbetta, 2000) one might predict that facilitated capture by emotional information would lead to relative benefits for emotional vs. neutral information in spatial memory. However the current findings suggest otherwise. Although emotional stimuli capture our spatial attention, we do not remember spatial locations any better when emotional stimuli are presented at to-beremembered locations. This may suggest a potential dissociation between spatial capture and memory, at least for emotional information. In addition to revealing a dissociation between capture and memory, the data point towards important differences between spatial and visual STM. While Jackson and colleagues (Jackson et al., 2008, 2009) showed that visual STM for face identity is enhanced when the faces were angry compared to happy or neutral, the current experiments showed no enhancement in spatial

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memory for emotional (angry, fearful or happy) compared to neutral faces. Taken together, our findings and those of Jackson et al. (2008, 2009) may imply that emotion affects visual, but not spatial, STM. Our findings are consistent with other evidence that STM visual and spatial memory are probably distinct mechanisms (Della Sala et al., 1999; Della Sala & Logie, 2002). Notably, in normal individuals, double dissociations are observed between visual and spatial spans, with spatial memory tasks being disrupted more by spatial interference than visual interference, while the reverse pattern is shown for visual memory tasks (Della Sala et al., 1999). There is also neuropsychological evidence of patients who have deficits in spatial, but not visual STM, or the opposite pattern (Della Sala & Logie, 2002). The finding that emotion did not influence spatial memory span suggests that ‘where’ (i.e. location only), not ‘what’ (i.e. meaning) is important in forming accurate representations in spatial working memory. In the saccadic eye movement condition, spatial span for the emotional face or emotional picture locations was not preserved and was reduced similar to that of neutral face/picture and baseline-condition locations. The finding that saccadic eye movements interfered with the maintenance of information in spatial working memory is consistent with previous studies (Lawrence et al., 2001; Lawrence, Myerson, & Abrams, 2004; Pearson & Sahraie, 2003; Postle et al., 2006) and supports Baddeley’s (1986) proposition that eye movement based rehearsal may subserve the maintenance of spatial information. That is, secondary tasks requiring eye movements may interrupt rehearsal, resulting in the loss of spatial information. The fact that eye movements disrupted spatial memory for all items is interesting as one might predict, based on previous literature showing that emotional biases exist in attention and memory (Cahill & McGaugh, 1998; Hamann, 2001; Yiend, 2009) that the emotional meaning of stimuli may be able to negate such a reduction. However, the results suggest that the disrupting effect of saccadic eye movements is so powerful that it can affect memory of stimuli which in other cognitive experimental tasks, have been found to dominate. This would suggest that in spatial working memory, bottom up processes win through, whereby saccadic eye movements affect temporary maintenance of location, over and above top-down influences such as the meaning that the stimuli hold to the observer. Why do concurrent saccadic eye movements produce such a severe reduction in participant’s spatial span across all conditions? One potential explanation may be related to saccadic remapping. In order to maintain a coherent percept of a visual scene while eye position continuously changes requires saccades to be accompanied by remapping of the visual environment (see review: Cavanagh et al., 2010). Thus each time we move our eyes, information is being remapped. Saccadic remapping has been found to influence spatial memory with decrements to spatial working memory performance being observed when participants are required to remap the visual array (Vasquez & Danckert, 2008). During retention in the current study participants were required to make multiple saccades, thus requiring space to be remapped several times. This may have led to a cost in memory performance for all items. Indeed, a comparison of the magnitude of the interference effect caused by saccadic eye movements shows that interference is greater when multiple saccades are executed (e.g. a 52% decrease in spatial span relative to fixation conditions: Pearson & Sahraie, 2003) rather than just a single saccade (e.g. a 38% decrease: Lawrence, Myerson, & Abrams, 2004). Therefore, the multiple saccades (and multiple remapping) required in the current task may have overridden top down influences such as the meaning of the stimuli. Notably, saccadic remapping is partly under the control of the superior colliculus (SC) (Sommer & Wurtz, 2006), a midbrain structure involved in eye movement control. Thus remapping by the SC may have produced interference in an oculomotor control network (Baddeley, 1986), disrupting the ‘where’ (i.e. location)

component of spatial memory. Moreover, the SC, along with the pulvinar in the thalamus, is involved in emotion processing via links with the amygdala (Anderson & Phelps, 2001; Le Doux, 1996). Activation of the amygdala may modulate hippocampal function, which may subsequently modulate consolidation processes (Cahill, 1999; McGaugh, 2000; McGaugh, Cahill, & Roozendall, 1996). This may provide a possible route whereby interference in the ‘where’ component by saccadic remapping, may have disrupted the ‘what’ component (i.e. meaning/emotional content) of spatial memory at an early stage. Alternatively, previous research with clinical populations (e.g. post traumatic stress disorder) has shown that saccadic eye movements can reduce the intensity of emotive images and memories (Shapiro, 1989). Notably, a patient is asked to hold in mind the most salient aspects of a traumatic memory, whilst making large magnitude saccadic eye movements. The saccadic eye movements result in reduction of anxiety and changes in the cognitive assessment of the memory (e.g. rated as less disturbing) (Andrade, Kavanagh, & Baddeley, 1997; Lee & Drummond, 2008; Lilley et al., 2009). It is possible that a similar effect may have occurred in the current study whereby saccadic eye movements reduced the valence of emotional stimuli appearing at to be remembered spatial locations to that of neutral face and non-face items, thus creating direct interference in the ‘what’ component. It is important to point out that in the current study we manipulated the emotional content of face stimuli during the encoding phase of a spatial memory task and found no differences in spatial span between emotional and neutral conditions. However it is possible that emotion may have influenced spatial span if emotional stimuli were presented as distracters during the retention interval (i.e. maintenance period). The logic being that attention might be captured more effectively by emotional (vs. neutral) distracters during retention, thus causing a stronger detrimental effect in spatial memory span. Several studies have examined how task irrelevant emotional stimuli influence working memory, often with inconsistent findings. For example, while some studies showed attenuated working memory performance with negative distracters (Dolcos, Kragel, Wang, & Mccarthy, 2006; Gray, Braver & Raichle, 2002), other studies have found better working memory performance when presented with emotional (vs. neutral distracters) (Erk, Kleczar & Walter, 2007) or no differences in working memory performance (Li, Li & Luo, 2006). While the current research was specifically designed to examine emotional modulation during the encoding phase in spatial memory, future research could examine the potentially disruptive effects of emotion during maintenance using the CBT. In conclusion, the current study showed that spatial span in the CBT was not modulated by emotion. Emotion neither enhanced span nor reduced the past saccadic deficit. Therefore, we propose that ‘where’ (i.e. location only), not ‘what’ (i.e. meaning) is important in forming accurate representations in spatial working memory. Acknowledgments We thank Mr. James Urquhart for technical support, Dr. Amelia Hunt for comments on earlier versions of the manuscript, and the Undergraduate Research Practical Groups for help with data collection. R.L.B. is supported by a Sixth Century Research Fellowship at the University of Aberdeen. E.V.T. was supported by a Summer Studentship from the Developing Scientists Fund at the University of Aberdeen. References Anderson, A. K., & Phelps, E. A. (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature, 411, 305–309.

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