Attentional orienting to mnemonic representations: Reduction of load-sensitive maintenance-related activity in the intraparietal sulcus

Neuropsychologia 50 (2012) 2805–2811

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Attentional orienting to mnemonic representations: Reduction of load-sensitive maintenance-related activity in the intraparietal sulcus ¨ Sabrina Trapp n, Joran Lepsien Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1a, 04103 Leipzig, Germany

a r t i c l e i n f o

abstract

Article history: Received 8 March 2012 Received in revised form 30 July 2012 Accepted 4 August 2012 Available online 13 August 2012

The orienting of attention to internal or mnemonic representations held in visual working memory (VWM) has recently become a field of increasing interest. While a number of studies support the hypothesis that attention to selected representations in VWM reduces memory load, conclusive findings are still missing. In this event-related functional magnetic resonance imaging (fMRI) study, we directly investigated whether attentional orienting to mnemonic representations reduces activity in VWM storage-related areas of the brain. VWM load was manipulated by asking subjects to memorize two, four or six items. A retro-cue during the subsequent delay period asked subjects to attend to just one of these items for a subsequent test. This was compared to trials where subjects were required to continue attending to all items for the subsequent test. Data show reduction of load-sensitive maintenance-related activity along the right intraparietal sulcus (IPS), directly linked to attentional orienting. While activity in the anterior IPS reflected the number of representations in the focus of attention, the activation pattern in the posterior IPS suggested residual activation related to unattended items. This dissociation is in line with a functional subdivision of the right IPS according to attentional and mnemonic properties. & 2012 Elsevier Ltd. All rights reserved.

Keywords: Attention Visual working memory Load Intraparietal sulcus Storage Rehearsal

1. Introduction Several authors conceptualize working memory (WM) as activated long-term memory (e.g., Anderson et al., 2004; Cowan, 1995; Ruchkin, Grafman, Cameron, & Berndt, 2003). Cowan (1999) assumes a circumscribed focus of attention that points to selected long-term representations, thereby modulating their accessibility for processing. The number of representations that can be included in the focus of attention varies among authors. McElree (2001) suggests a bipartite architecture in which he differentiates between long-term representations and a single representation in the focus of attention. Oberauer (2002) assumes a tripartite architecture, with a zone of activated long-term memory, a region of direct access with a limited number of representations, and a focus of attention, which is restricted to one representation. Although there is broad consensus about the processing benefits for representations in the focus of attention, less is known about the underlying neural dynamics that cause these advantages. Generally, the ‘‘sticking out’’ of attended stimuli might be due to a spotlight process, i.e., an enhancement of selected items. In the perceptual domain, for instance, orienting attention to visual stimuli has been shown to

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result in enhanced functional magnetic resonance imaging (fMRI) signals in several areas of the visual cortex (Brefczynski & DeYoe, 1999; Kastner, De Weerd, Desimone, & Ungerleider, 1998; Martinez et al., 1999; O’Craven, Downing, & Kanwisher, 1999; Somers, Dale, Seiffert, & Tootell, 1999); including categoryspecific areas, such as the parahippocampal place area (PPA) and the fusiform face area (FFA; O’Craven et al., 1999). Alternatively, the reduction and/or suppression of activity related to unattended representations could cause a greater salience of attended items, thereby facilitating processing. Finally, a mixture of both options is possible. The orientation of attention to mnemonic representations has been investigated by presenting a cue during the retention period of a WM task which instructs subjects to orient attention to a single representation held on-line in WM (‘‘retro-cue’’, Griffin & Nobre, 2003; Landman, Spekreijse, & Lamme, 2003). Compared to trials without orienting attention, there are improvements in performance as well as attention-related modulations in electrophysiological markers (Griffin & Nobre, 2003). Further studies identified closely overlapping networks for attentional orienting to physical stimuli and mnemonic representations (Nee & Jonides, 2009; Nobre et al., 2004). There are studies that report persistent activity in the FFA and the PPA when faces and scenes are maintained in visual WM (VWM) (Ranganath, DeGutis, & D’Esposito, 2004), with activity increasing with the number of faces held on-line

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(Druzgal & D’Esposito, 2001, 2003).1 Lepsien and Nobre (2007) demonstrated that maintenance-related activity in the FFA and PPA was modulated towards the type of information that was selected into the focus of attention (i.e., faces or scenes). These modulations were directly related to the behavioral benefits of attentional orienting. In a follow-up study, Lepsien, Thornton, and Nobre (2011) reported an interaction in several brain areas between attentional orienting and the amount of faces [scenes] held on-line, suggesting that attention modulates VWM load. This idea is also supported by a study that demonstrated a modulation of the ‘‘contralateral delay activity’’ (CDA). This lateralized ERP marker is sensitive to the amount of information in VWM (Vogel & Machizawa, 2004). The CDA was reduced in conditions of attentional orienting (Kuo, Stokes, & Nobre, 2012). Similarly, Nobre, Griffin, and Rao (2008) identified an ERP component that was associated with searching for an item within VWM at test phase. While this component systematically varied with the amount of information maintained in VWM, it was absent when retro-cues for attentional orienting were provided during the retention period. The authors suggested that attending to mental representations facilitates search through the memory store, with the effect that the ‘‘load of the maintained array [y] shrinks around the retro-cued item.’’ (p. 7). Together, these studies provide evidence that facilitative effects of attentional orienting are due to a release of unattended information. However, to date, there is no straightforward demonstration that load-sensitive maintenance activity in the brain, related to storage of visual information, is reduced due to attentional orienting. One problem with previous studies investigating modulations of maintenance-related activity in category-sensitive areas, such as PPA and FFA (Lepsien & Nobre, 2007; Lepsien et al., 2011; Leung et al., 2009) is that the anticipatory effects of expecting a category can also lead to modulation of activity in these areas (Esterman & Yantis, 2010; Puri, Wojciulik, & Ranganath, 2009), potentially masking effects of attention (for a critical discussion of the mesh between attention and expectation see Summerfield & Egner, 2009). Indeed, Lepsien et al. (2011) demonstrated such expectancy-based effects in PPA and FFA, when categorical retro-cues were pointed towards faces or scenes held in VWM, with the ratio of scenes to faces varying in each trial. While activity in several brain areas reflected the VWM load after attentional orienting, i.e., the task-relevant amount of stimuli in the focus of attention, a load-independent pattern was found in the PPA and the FFA, strongly suggesting that expectancy effects were dominating the patterns of activity in previous studies. In order to circumvent these pitfalls, the present study avoided use of stimulus categories. In addition, because attention-related enhancement or reduction can only be inferred when compared to a baseline condition, the present study included a control condition without attentional orienting. In this study, stimuli were arranged in a spatial manner with the effect that both the identity and the location of the stimuli had to be remembered. There is evidence that the intraparietal sulcus (IPS) is involved in the storage of visuo-spatial information (Harrison, Jolicoeur, & Marois, 2010; Xu & Chun, 2006). The bloodoxygen-level-dependent (BOLD) response in this region not only correlates with the amount of objects subjects were able to maintain in VWM, but also reaches a plateau after four objects (Todd & Marois, 2004), which is estimated to be the capacity limit in humans (Cowan, 2001). Additionally, it has been suggested that the IPS is involved in attention-based rehearsal rather than the storage of information (Magen, Emmanouil, McMains,

1 The amount of representations maintained in WM is often referred to as the ‘‘load’’. Therefore, the concept of load refers to all processes that are necessary for the active maintenance and rehearsal of this information.

Kastner, & Treisman, 2009). Activation in the IPS would therefore qualify as providing neural evidence of a reduction of loadsensitive maintenance activity. Such a reduction would indicate reduced VWM load, either in storage or attention-based rehearsal. In the first experiment, fMRI was utilized to identify areas during the maintenance period that show both increase in activity with increasing VWM load, and at the same time show reduced activity in conditions of attentional orienting. To this end, the VWM load (amount of to-be-memorized items) was varied. We expected an interaction between the initial VWM load and attentional orienting, i.e., pronounced (reductive) effects with increasing VWM load in retro-cue conditions. The second experiment used behavioral measures to test to what extent the spatial configuration of the array during encoding influences the subsequent release of irrelevant information from VWM. 2. Methods 2.1. Experiment 1 2.1.1. Materials and procedure 2.1.1.1. Participants. Twenty-four neurologically intact subjects (mean age 25.3 years, SD¼2.1, 10 females) took part in the study after informed written consent had been obtained in accordance with guidelines of the local ethics committee. These volunteers were recruited from the Max Planck Institute for Human Cognitive and Brain Sciences and were financially compensated for their participation. All participants had normal or corrected to normal vision. 2.1.1.2. Visual short-term memory task. We used a variant of the change-detection task, consisting of an encoding, a delay and a recognition phase, with a retro-cue embedded in the delay phase (Fig. 1). The 100% valid retro-cue instructed subjects to select just one item for further processing. Participants were informed that whenever a retro-cue was presented, it was always 100% valid. In other words, a potential change (50%) would only occur on the position of the retro-cued item, and other items would never change. In case of no cue, participants had to select all items for further processing. A potential change (i.e., a new item, 50%) could then occur on every position. At the beginning of the memory task, subjects saw a small hexagon which served as a fixation point in the middle of the screen. In the encoding phase, two, four or six black, umbrella-like objects (provided by Xu & Chun, 2006) were presented simultaneously. These were configured in an imagery circle at approximately an 8.91 subtending visual angle, at pseudorandom positions, for 1000 ms on a light gray background. A short delay phase followed (2000 ms), during which participants were required to remember all objects and their positions. Subsequently, either an informative retro-cue (selection) or an uninformative cue (no-selection) was presented. In the selection condition, one side of the hexagon turned red for 500 ms. Participants were instructed to focus in their mind the object that was placed at this position and maintain it as a target for the subsequent recognition test. In the no-selection condition, the whole hexagon turned red for 500 ms. Subjects had to memorize all items for the subsequent recognition test. The test display followed after another, variable delay phase (6000, 7000, 8000, 9000 or 10,000 ms). In the test phase, the full array of two, four or six objects in the same spatial layout as in the encoding phase was presented for 500 ms as a probe. Participants were asked to determine whether the probe array was identical to the initial array, or whether it had changed, by pressing the left key for ‘‘same’’ and the right key for ‘‘different’’. Speed and accuracy were both emphasized. Subjects received feedback about the correctness of their performance (‘‘right’’ or ‘‘wrong’’) after each trial. To minimize verbal recoding, participants were required to rehearse four digits throughout the VWM task. The digits were specified at the beginning of each block for 1000 ms. Compliance was assessed by a delayed-match-to-sample task at the end of each trial, which asked whether a single digit has been presented or not. Subjects received feedback on their response after each trial. The experiment included 2 consecutive sessions, each consisting of 90 trials. One session lasted about 40 minutes. 2.1.2. fMRI data recording and analysis Subjects lay on their back inside a 3 T Bruker Medspec 30/100 scanner and viewed the stimuli via a mirror projected onto a back-projection screen by an LCD projector. Stimulus presentation and behavioral response collection were controlled by Presentation software (Neurobehavioral Systems, Inc., version 12.7). Thirty-two axial slices (19.2 cm FOV, 64  64 matrix, 3 mm isotropic voxel, 1 mm spacing), were collected parallel to the AC–PC plane with a gradient echo pulse sequence (TE¼ 25 ms, TR¼2 s).

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Fig. 1. Retro-cue task. Red: Articulatory Suppression. Subjects saw four digits that they were required to subvocally rehearse over the course of the trial in order to respond to a delayed-match-to sample task at the end. Blue: Visual Change Detection Task. Two, four or six umbrella-like, non-colored stimuli were presented. After a fixed delay of 2 s, (i) a 100% valid retro-cue indicated to select just one of these items and maintain it for further processing (selection, top) or (ii) all items were marked as relevant for further processing (no selection, bottom). This was followed by a variable delay, after which subjects judged whether the probe display was same or different from the stimulus array. Subjects received feedback after each trial. present study focused on the maintenance period after cue presentation (ISI 2). This period was modeled using six separate regressors: selection_VWM_load_2, selection_VWM_load_4, selection_VWM_load_6, no_selection_VWM_load_2, no_selection_VWM_load_4, no_selection_VWM_load_6. We also included error trials as a regressor of no interest into the model (incorrect response, late response, no response), modeled as extended events with the duration comprising the length of the whole trial. The intertrial intervals contributed to the implicit-baseline condition. The events were then convolved with a synthetic hemodynamic response function (Friston et al., 1998). The results of the first-level analyses were entered into a second-level flexible-factorial analysis with subjects as a random factor. The statistical SPM(t) maps were thresholded at p o 0.05 [family wise error (FWE) corrected] with a minimal cluster size of five voxels. Rfxplot toolbox (http://rfxplot.sourceforge.net) was used to extract and plot the contrast estimates for the maintenance-related activity during ISI2.

2.1.3. Results Note that attentional orienting was always restricted to a single item. Because the amount of irrelevant material varied with VMW load, we expected the facilitative effects of retro-cueing to be differentially pronounced. More specifically, we expected that the difference between selection and no-selection would be most pronounced with six memorized objects and least with two objects. Statistically, these patterns translate into an ordinal interaction. 2.1.3.1. Behavioral data. Two subjects were excluded from the analysis due to high error rates in all conditions (overall accuracy: 45% and 39%). Responses below 200 ms and longer than 2000 ms were considered as outliers and were excluded from the analysis (o 2.5% on average). A repeated-measures analysis of variance (ANOVA) tested the influence of attentional orienting (selection, no-selection) and VWM load (2, 4, 6 objects) upon mean reaction time (RT) and accuracies (AC). Only trials with correct responses were included in the analysis of the RT data.

Fig. 2. Behavioral data for the visual working memory (VWM) task. (A) Reaction times (with7 standard error of the mean, SEM) revealed an increase with VWM load and subjects were able to profit from the retro-cue. However, the interaction between attention and VWM load was not significant. (B) Accuracies (with 7 SEM) show a comparable pattern, again without a significant interaction.

The main experiment was split into two consecutive sessions, each consisting of one run, with a delay of approximately one week between sessions. Within each session, 1225 volumes were acquired. High-resolution T1-weigheted MR scans of the subjects were acquired beforehand in a separate session. FMRI data were analyzed using Statistical Parametric Mapping (SPM8). The preprocessing was done with the following steps: slice-time correction, realignment, correction for field inhomogenities (unwarping) and normalization to the Montreal Neurological Institute (MNI) template, using the unified segmentation approach (Ashburner & Friston, 2005), and spatial smoothing with an 8 mm Gaussian kernel. A high-pass filter was applied to eliminate slow signal drifts (128 Hz cutoff frequency). For the design matrix, we modeled extended events (preparation period, memory display þISI 1, cue, ISI 2 and response phase). The

For both RT and AC the main effect of VWM load reached significance (RT: F2,42 ¼ 6.76, p ¼0.003; AC: F2,42 ¼ 54.73, p o 0.001) as well as the main effect of attentional orienting (RT: F1,21 ¼ 21.07, p o 0.001; AC: F1,21 ¼ 22.19, p o0.001). Participants were significantly slower and less accurate as the amount of memorized information increased, and were able to use the retro-cue to improve their performance. Contrary to our hypothesis, the ANOVAs did not reveal significant interactions between attentional orienting and VWM load, neither for RT (F2,42 ¼0.94, p ¼0.398) nor for AC(F2,42 ¼0.107, p ¼0.899), i.e. the performance benefit induced by the informative as compared to the uninformative cue did not significantly differ between numbers of objects in VWM. Performance in the articulatory suppression task was high (2 objects ¼92%; 4 objects¼ 91%; 6 objects¼ 90%). The statistical analysis of AC data revealed no main effect of VWM load (F2,42 ¼ 0.64, p ¼0.532), attentional orienting (F1,21 ¼ 1.13, p¼ 0.299), and no significant interaction (F2,42 ¼ 0.84, p ¼0.441), indicating that the articulatory suppression task did not interfere with the VWM task. 2.1.3.2. Neuroimaging data. The analysis of the fMRI data was performed in two steps. First, we probed for the ordinal interaction between attentional orienting and VWM load on whole-brain level. This contrast revealed a significant activation in a circumscribed region in the right anterior IPS (MNI coordinates: x¼ 45; y¼  34; z¼ 43; voxel size¼81; z¼5.32), adjacent to the postcentral sulcus (see Fig. 3, in red). Here, activation increased with increasing VWM load but showed no such load

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Fig. 3. Maintenance activity after cue presentation (ISI 2). Yellow¼ load-sensitive maintenance activity. Both anterior and posterior parts of the IPS are activated. Red¼ interaction of visual working memory load x attentional orienting. Only the anterior IPS is activated. Displays are oriented following the neurological convention (left¼ left). The numbers indicate the stereotactic coordinates of the sagittal, coronal and axial planes, respectively.

Table 1 MNI-Coordinates, maximum z-values, spatial extent and labels of significantly activated brain areas f visual working memory load (thresholded at p o 0.001 uncorrected, with a minimal cluster size of five voxels). H ¼ hemisphere, L ¼left, R¼right, IPS ¼intraparietal sulcus, AG ¼ angular gyrus, CG¼ cingulate gyrus, IPS¼ intraparietal sulcus, MOG¼ middle occipital gyrus. Area

H

x

y

z

Voxel

Z

AG MOG CG Putamen

R R R R L R R

45 66 6 18  18 45 21

 52  22  34 5 8  40  70

28  11 31  11  14 55 55

68 55 94 24 13 24 6

4.09 4.01 3.93 3.61 3.34 3.54 3.20

Anterior IPS Posterior IPS

reduced to the amount of relevant information in the focus of attention, i.e., only one item. In order to support these different effects in anterior and posterior IPS statistically, post-hoc tests were conducted. To this end, a region-of-interest (ROI) analysis of anterior and posterior IPS was performed. Based on the contrast of ordinal interaction and VWM load, respectively, spherical ROIs with a radius of 3 mm were created around coordinates of the single peak activation. Then, contrast estimates of the selection condition were extracted and compared using a one-way repeated measurement ANOVA with VWM load as within-subject factor (2, 4, 6 objects). As expected, the results showed no effect of VWM load for the anterior IPS in the selection condition (F2,42 ¼0.96, p ¼0.393). In contrast, the effect of VWM load for the selection condition turned out to be significant in the posterior IPS (F2,42 ¼ 4.82, p ¼0.013). In a second step, the same analysis was conducted for the no-selection condition. Here, the effect of VWM load was significant both for the right anterior (F2,42 ¼5.42, p¼ 0.008) and posterior IPS (F2,42 ¼4.82, p ¼0.003). Fig. 4. Contrast estimates (with7 standard error of the mean). (A) Whole brain analysis, right anterior IPS. Activation profile shows an increase of activation with increasing visual working memory (VWM) load in conditions of no-selection and no such increase in conditions of selection. (B) Whole brain analysis, right posterior IPS. Activation profile shows an increase of activation with increasing VWM load both in conditions of no-selection and selection. effect when only one item had to be selected (see Fig. 4A). The activation was much more anterior to the region which has previously been described as showing storage-related activity (Todd & Marois, 2004). However, previous studies have not used the retro-cue as an additional manipulation. Therefore, in a second step, we probed for the effect of VWM load only in the no-selection condition. This contrast revealed no significant activation clusters. At a lower threshold (p o0.001 uncorrected), activation peaks in the right angular gyrus, right middle temporal gyrus, right cingulate gyrus, bilateral putamen, and right anterior and posterior IPS were identified (see Table 1 and Fig. 3, in yellow). The peak coordinates of the posterior IPS were closer to those which have been reported in the context of storage-related VWM activity (Todd & Marois, 2004). As can be seen in Fig. 4B, activity in the posterior IPS not only increased with increasing VWM load in the no-selection, but also in the selection condition. In other words, activation was not

2.2. Experiment 2 In experiment 1, the interaction between VWM load and attentional orienting did not reach significance for the analyses of the behavioral data and the posterior IPS. The interaction was significant only for the right anterior IPS. Since the data indicate that participants were able to use the retro-cue (resulting in a clear performance benefit), different activation patterns in subareas of the IPS are unlikely to be due to unsuccessful experimental manipulation. One likely explanation for the observed pattern is that irrelevant information from VWM was not fully released (although it might have not been actively rehearsed either), resulting in residual activation in storage-relevant areas (posterior IPS). As a consequence, this residual information might interfere with relevant items at retrieval, thereby slowing reaction time and decreasing accuracy with increasing VWM load in conditions of attentional orienting, as was observed in the behavioral data (see Fig. 2). Such an incomplete release could be due to the way the information was presented at encoding. In experiment 1, all items were presented simultaneously, both during the encoding phase and the test phase. It is known that spatial layout or relational information is stored automatically in VWM, particularly with whole-display configurations (Jiang, Olson, & Chun, 2000). Hence, the single items and/or layout information of these items might have been

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Fig. 6. Comparison of selection efficiency between parallel (experiment 1) and sequential (experiment 2) encoding. Y-axis shows the percentage reduction in reaction time in conditions of selection. The reduction was more accentuated with sequential stimulus encoding at high visual working memory load.

Fig. 5. Behavioral data for the visual working memory (VWM) experiment with sequential stimulus presentation. (A) Reaction times (RT, with 7 standard error of the mean, SEM). (B) Accuracies (AC, with 7SEM). Both RT and AC show main effects of attentional orienting, VWM load and a significant interaction between attentional orienting and VWM load. grouped and subsequently been stored together. Perhaps, it is not possible to select just a part of such a ‘‘cluster’’ representation, because other features will be automatically selected, too. This might have hampered the release of irrelevant information from VWM, rendering the effect of attentional orienting much smaller than would be expected at high VWM load. To test this hypothesis, in experiment 2 items were presented sequentially during the encoding phase. 2.2.1. Material and procedure 2.2.1.1. Participants. Ten neurologically intact subjects (mean age 23.9 years, SD¼ 2.9) gave informed consent to participate in the study. These volunteers did not participate in experiment 1, were recruited from the Max Planck Institute for Human Cognitive and Brain Sciences and were financially compensated for their participation. All participants had normal or corrected to normal vision. 2.2.1.2. Visual short-term memory task. The task was identical to experiment 1, except that stimuli were presented sequentially (two, four or six), in random order, during the encoding phase (200 ms per stimulus). We closely followed the procedure of Xu and Chun (2006), who also compared parallel with sequential stimulus presentation. In their study, the complete display was presented for 200 ms and a single stimulus in the sequential condition for 50 ms. In the present study, total presentation time for whole displays was slightly modified because our experiment was more difficult and additionally had the retro-cue manipulation and longer maintenance periods. 2.2.2. Results and discussion One subject was excluded from the analysis due to exceptionally high error rates in all conditions (overall accuracy: 33%). Responses below 200 ms and longer than 2000 ms were considered as outliers and were excluded from the analysis (o 2% on average). A repeated-measures ANOVA revealed a main effect of attentional orienting, with faster RT (F1,8 ¼ 25.99, p o 0.001) and higher accuracies (F1,8 ¼10.99, p¼ 0.011) in selection conditions. Furthermore, the effect of VWM load reached statistical significance both for RT (F2,16 ¼ 44.15, p o 0.001) and AC (F1,16 ¼ 25.31, p o0.001). Most importantly, the interaction between attentional orienting and VWM load was significant for RT (F2,16 ¼ 6.12, p ¼ 0.011) and AC (F2,16 ¼ 4.7, p ¼ 0.025).

In order to compare the selection efficiency between experiments 1 and 2, the data were analyzed in a mixed model ANOVA with VWM load as a within-subjects factor (2, 4, 6 objects) and encoding strategy (parallel, sequential) as a between-subject factor. It has been suggested that speed at retrieval can be considered as an indicator of the amount of information maintained in short-term memory (Sternberg, 1966). Therefore, percentage reduction in speed (RT) due to attentional orienting was calculated as a dependent variable (100 [RTselection/RTno selection]  100). The results show a significant effect of VWM load (F2,58 ¼7.55, po0.001). Bonferroni corrected post-hoc-tests revealed a significant difference between VWM load two and four (po0.001). The difference between VWM load four and six (p¼0.245) and two and six (p¼ 0.181) was not significant. Furthermore, there was a main effect of encoding strategy: selection efficiency was higher when stimuli were presented sequentially (F1,29 ¼ 7.89, p¼0.009). The interaction between VWM load and encoding strategy was also significant (F2,58 ¼5.37, p¼0.007). This was due to higher selection efficiency for sequential encoding at VWM load four and six (see Fig. 6). The analysis clearly demonstrates that selection efficiency is higher when stimuli are presented sequentially at encoding. Furthermore, data show that the difference between parallel and sequential encoding increases with VMW load. The lack of difference between parallel and sequential encoding at VWM load two might be due to a ceiling effect, since overall accuracy was very high for both conditions (parallel: 87% correct; sequential: 86% correct for selection condition). Furthermore, there was a drop in selection efficiency in the highest VWM load condition (six objects). Human WM capacity is usually assumed to reach a plateau around four objects (Cowan, 2001). In line with this limit, the accuracy was generally very low for this condition (see Figs. 3B and 5B). Therefore, the data might be confounded with task-independent processes, such as guessing.

3. General discussion Recent studies have demonstrated that attentional orienting reduces VWM load and leads to performance benefits (Nobre et al., 2008; Kuo et al., 2012; Lepsien et al., 2005, 2011). By using fMRI, the present study aimed to further elucidate the underlying neural mechanisms of this effect, and probed for storage-relevant brain areas that show such reductive effects in conditions of attentional orienting. Subjects were required to memorize either two, four or six objects in a VWM task. Reductive effects were expected to be most accentuated in conditions with six objects, where the amount of irrelevant material was the highest. A whole-brain analysis revealed a cluster in the anterior end of the IPS that corresponded to such a pattern. Several studies have suggested that this region constitutes the source for attentional

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control signals which modulate activity elsewhere in the cortex. For example, Thakral and Slotnick (2009) examined neural correlates of spatial attentional orienting and found the anterior IPS to be related to sustaining the attentional focus. Culham, Cavanagh, and Kanwisher (2001) parametrically varied the amount of information that needed to be attended to in a multiple-object tracking task. Here, the anterior IPS was sensitive to an increase in attentional demands, excluding its role in more task-specific processes (see Jovicich et al., 2001 for similar results). Directly supporting this account, Lepsien et al. (2011) reported a virtually identical region in the right anterior IPS which showed an activation pattern reflecting changes in the VWM load, but did not show activity related to storing visual information. In a study by Majerus et al. (2007), subjects had to memorize either the identity or the order of stimuli for a VWM task. The authors found that the left anterior IPS was activated in both conditions, indicating a more general, attentional role, as opposed to a specific role in storage of information. Our data suggest that these top-down control signals can be dynamically adapted ‘‘on-line’’ to the task at hand. Behavioral data did not reveal more pronounced differences between selection and no-selection conditions at higher VWM load, i.e., no interaction between attentional orienting and VWM load. One possible explanation is that residual information influenced performance, opposing exhaustive facilitative effects of attentional orienting. This interpretation fits well with the activation profile of the posterior IPS. Here, brain activity in conditions of attentional orienting depended on the amount of previously stored information. The activation spot of the posterior IPS was adjacent to the region which has been suggested to be involved in storage of VWM information (Todd & Marois, 2004; Xu & Chun, 2006). Thus, the activation profile in the posterior IPS in our study might mirror a residual storage of irrelevant information, i.e., representations that were not chosen by the retro-cue. Given that material was presented simultaneously and in a spatial manner at encoding (experiment 1), it was speculated that grouping might have hampered the selection of single items. This hypothesis was supported by showing the expected interaction between attentional orienting and VWM load when information was presented sequentially at encoding (experiment 2). A direct comparison of selection efficiency between both experiments clearly demonstrated stronger effects of attentional orienting when stimuli were presented sequentially at encoding. Thus, based on behavioral data from these two experiments, a significant interaction can be predicted for the activation profile in the posterior IPS when information is presented sequentially. In this case, activation should demonstrate the same profile as in the anterior IPS. Albeit an interesting issue, the exact representational format of the information maintained in VWM cannot unequivocally be determined with this study. There are, however, some studies that aim to specify the format of information maintained in the posterior IPS, which seems to relate to spatial rather than identity information (Harrison et al., 2010). In future studies, it has to be addressed whether residual information represents general layout or refers to single locations, and how exactly the representational format and activation strength differs between selected items, non-selected but not successfully released items and successfully released items. The exact function of the IPS for VWM has been a matter of controversy. In opposition to visuo-spatial storage accounts of the IPS, it has been suggested that its role relates more to attentional demands and rehearsal processes (Magen et al., 2009). The statistical dissociation between the anterior and the posterior IPS in this study invites a potential functional subdivision and therefore offers a compromise between the two positions. However, future studies

need to directly manipulate and disentangle storage and rehearsal processes and relate these functions to activity in the IPS. The data presented here also add further evidence that filtering of irrelevant material is an important feature for efficient WM functioning. For example, Vogel, McCollough, and Machizawa (2005) identified high performers in a VWM task as subjects who were primarily able to ignore irrelevant information. While neurophysiological correlates of these subjects mirrored the required amount of information, i.e., the number of stimuli they were asked to encode for the task, low performers showed indices of additional memory load due to encoding of irrelevant material. Similarly, Zanto and Gazzaley (2009) found suppression during encoding to be intimately related to performance in a VWM task. It seems that filtering irrelevant material at encoding is a major cognitive building block that accounts for VWM performance differences between subjects (Bor & Owen, 2006; Cowan & Morey, 2006). As of yet, these conclusions have been restricted to the encoding phase. However, this study suggests that these processes continue to be important at further VWM stages, i.e., maintenance and rehearsal of information (see also Kuo et al., 2012). Further studies are needed to examine individual differences in attention-related reduction of VWM load in more detail, i.e., examine links between brain and behavioral data.

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