Exp Brain Res (2011) 212:293–304 DOI 10.1007/s00221-011-2730-z
R ES EA R C H A R TI CLE
Attention does more than modulate suppressive interactions: attending to multiple items Paige E. Scalf · Chandramalika Basak · Diane M. Beck
Received: 20 December 2010 / Accepted: 8 May 2011 / Published online: 4 June 2011 © Springer-Verlag 2011
Abstract Directing attention to a visual item enhances its representations, making it more likely to guide behavior (Corbetta et al. 1991). Attention is thought to produce this enhancement by biasing suppressive interactions among multiple items in visual cortex in favor of the attended item (e.g., Desimone and Duncan 1995; Reynolds and Heeger 2009). We ask whether target enhancement and modulation of suppressive interactions are in fact inextricably linked or whether they can be decoupled. In particular, we ask whether simultaneously directing attention to multiple items may be one means of dissociating the inXuence of attention-related enhancement from the eVects of inter-item suppression. When multiple items are attended, suppressive interactions in visual cortex limit the eVectiveness with which attention may act on their representations, presumably because “biasing” the interactions in favor of a single item is no longer possible (Scalf and Beck 2010). In this experiment, we directly investigate whether applying attention to multiple competing stimulus items has any inXuence on either their evoked signal or their suppressive interactions. Both BOLD signal evoked by the items in V4 and behavioral responses to those items were signiWcantly compromised by simultaneous presentation relative to simulta-
P. E. Scalf (&) · D. M. Beck Beckman Institute, University of Illinois at Urbana-Champaign, 405 N Mathews, Urbana, IL 61801, USA e-mail:
[email protected] C. Basak Department of Psychology, Rice University, Houston, TX, USA D. M. Beck Department of Psychology, University of Illinois at Urbana-Champaign, 603 East Daniels Street, Champaign, IL 61820, USA
neous presentation, indicating that when the items appeared at the same time, they interacted in a mutually suppressive manner that compromised their ability to guide behavior. Attention signiWcantly enhanced signal in V4. The attentional status of the items, however, had no inXuence on the suppressive eVects of simultaneous presentation. To our knowledge, these data are the Wrst to explicitly decouple the eVects of top-down attention from those of inter-item suppression. Keywords Attention · Vision · fMRI · Biased competition
Introduction One of the many functions of attention is to enhance the perceptual representations of task-relevant items so that they are more likely to guide behavior (Luck and Thomas 1999; Corbetta et al. 1991; for a review see Luck and Vecera 2002). If we conceive of this type of attention simply as an enhancing “spotlight”, it is easy to imagine that it could be applied to multiple and single items in a similar manner that produces similar eVects on those items’ representation in visual cortex (Brefczynski and DeYoe 1999; McMains and Somers 2004; McMains and Somers 2005). Attention, however, acts on striate and extrastriate representations via a number of complex mechanisms; for example, one mechanism by which attention prioritizes task-relevant material is to modulate suppressive interactions with neighboring stimuli in visual cortex such that it reduces their impact on the response to the task relevant stimulus (Kastner et al. 1998; Reynolds et al. 1999; Sundberg et al. 2009; Lee and Maunsell 2010). When attention is directed toward multiple items, however, attention may be less able
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to bias the suppressive interactions in favor of any one stimulus (Scalf and Beck 2010). Such a situation raises the possibility that the eVects of directing attention and biasing suppressive interactions could be decoupled. In particular, we ask whether directing attention to multiple items results in (a) any attention-related enhancement and (b) any modulation of suppressive interactions. Both single cell and fMRI data indicate that directing attention to a visual item enhances the response it evokes in the visual system; this enhanced response is widely believed to reXect a stronger sensory representation of the item (for review see Treue 2001; Kastner and Pinsk 2004). Single unit recording data, for example, indicates that when a V4 cell’s preferred stimulus falls within its receptive Weld (RF), the cell Wres even more strongly when attention is directed to that item as opposed to another item (Moran and Desimone 1985; Connor et al. 1997; Lee and Maunsell 2010). Similarly, blood oxygen level dependent (BOLD) striate and extrastriate signals associated with the sensory representation of a stimulus are enhanced if attention is directed toward the spatial location containing that stimulus (Brefczynski and DeYoe 1999; Tootell et al. 1998; McMains et al. 2007; McMains and Somers 2004; Kastner et al. 1998). Attention, then, acts to enhance the striate and extrastriate representations of attended material. One mechanism by which attention enhances signal is by biasing suppressive interactions in favor of the task relevant stimuli and against task-irrelevant stimuli (Bles et al. 2006; Kastner et al. 1998; Scalf and Beck 2010). When neighboring stimuli are presented simultaneously, their representations interact in a mutually suppressive manner, causing them to be weaker (i.e., signaled less clearly) than those of individually presented stimuli (Allman et al. 1985; DeAngelis et al. 1992; Blakemore and Tobin 1972; Snowden et al. 1991; Carandini et al. 1997; Rolls and Tovee 1995; Miller et al. 1993; Zoccolan et al. 2005; for a review, see Heeger 1992). For example, two stimuli presented simultaneously within the receptive Weld (RF) of a cell will evoke activity intermediate to that evoked by each stimulus presented in isolation (Chelazzi et al. 1998, 2001; Reynolds and Desimone 1999; Snowden et al. 2001, Lee and Maunsell 2010). Mutually suppressive interactions between the two stimuli, then, each pull the response of the cell in diVerent directions such that neither wins that competition, and the result is a cell that signals neither stimulus clearly. Similarly, the blood oxygen level dependent (BOLD) responses evoked in V4 by four neighboring stimuli are greater when they are presented sequentially (and are unable to spatially interact with one another) than when they are presented simultaneously (and are able to interact with one another) (Kastner et al. 1998, 2001; Beck and Kastner 2005, 2007). Directing top-down attention to one of the competing representations, however, modulates its suppressive inter-
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actions with other stimuli such that the attended item dominates the neural response. SpeciWcally, when attention is directed to one of two items in a cell’s RF, the response of the cell is heavily weighted in favor of the attended stimulus such that the response to the pair of stimuli is more similar to the response to the attended stimulus alone (Chelazzi et al. 1998, 2001; Lee and Maunsell 2010; Recanzone and Wurtz 2000; Reynolds et al. 1999). BOLD signal diVerence between sequential and simultaneous presentation of four items is also reduced when attention is directed to one of the items (Bles et al. 2006; Kastner et al. 1998). Attention then is thought to bias mutually suppressive interactions in favor of the attended stimulus, such that suppressive eVects of the attended stimulus on unattended stimuli are increased, while the suppressive eVects of unattended stimuli on the attended stimulus are decreased. Similar eVects are predicted by divisive normalization models of attention (Lee and Maunsell 2009; Reynolds and Heeger 2009). The net eVect of this attentional biasing process is an enhanced representation of the attended stimulus, at the expense of the unattended stimuli, that is strong enough to guide behavior. Consequently, attention is most eVective at enhancing stimulus representations when those representations must overcome suppressive inXuences to guide behavior (e.g., Kastner et al. 1998; Reynolds and Desimone 2003; Bles et al. 2006; Reynolds et al. 1999). Our previous work (Scalf and Beck 2010) suggests that there are conditions in which top-down biasing may be unable to resolve suppressive interactions; speciWcally, this may occur when attention must be directed to multiple stimuli. In this case, multiple competing items would be task relevant; any bias in favor of a single task-relevant item at the expense of the other items would be counteracted by an equivalent bias in their favor. In other words, the attended items should continue to mutually suppress one another. Indeed, our previous work suggests that the inXuence of attention on multiple items is reduced when those items are positioned such that they interact in V4 (Scalf and Beck 2010). When participants attended to items that likely suppress one another’s representations in V4 (i.e., presented simultaneously in the upper-right visual quadrant, center-to-center separation of 2°), signal evoked by an attended item was higher if it was the sole recipient of attention than if it was one of multiple attended neighboring stimuli. When participants attend to items that were unlikely to suppress one another’s representations in V4, however, signal to an attended item was insensitive to whether or not that item was the sole recipient of attention. When attention was directed to multiple items, then, their potential to suppress one another reduced attention’s ability to enhance their V4 representations. These data raise two interesting questions. First, does directing attention to multiple items result in any modula-
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tion of the suppressive interactions among them? In particular, we ask whether suppressive interactions among multiple attended stimuli are reduced compared to when attention is directed away from those items. Second, if attention is unable to reduce suppressive interactions among multiple attended items, does it have any eVect at all? In other words, might attention enhance signal to multiple attended items while still failing to modulate suppressive interactions among those items? This raises the possibility that attention is unable to reduce suppressive interactions among multiple items if it is applied to those items simultaneously. We presented stimuli in Wve locations in the upper-right visual quadrant under conditions either likely (simultaneous presentation) or unlikely (sequential presentation) to produce mutually suppressive interactions among stimuli. Participants maintained Wxation at all times on an RSVP stream of letters, digits, and symbols. In order to determine whether attention enhanced the signal evoked by the upperright visual Weld items, we compared this signal under conditions in which participants attended to Wxation (and monitored the RSVP stream for a lower case “a” and thus the Wve stimuli were unattended) or attended to Wve of the items (and searched for a color/shape/texture conjunction in any of the Wve locations). In order to determine whether attention is able to reduce suppressive interactions among multiple stimuli to which it is simultaneously applied, we compared the BOLD signal evoked in V4 for sequential versus simultaneous presentations under attend-Wxation and attend-Wve conditions. If attention reduces suppressive interactions among attended items, then presentation method (sequential and simultaneous) and attentional condition (attend Wxation, attend Wve) should interact such that the diVerence between sequential and simultaneous presentation conditions is smaller when the items are attended than when they are unattended. In this case, suppression indices (a baseline-independent quantiWcation of the ratio of activation under sequential and simultaneous presentation conditions) should be higher for unattended than attended conditions. We note that this pattern of results would be similar to those reported under conditions in which participants alternate between attending to a single location and attending to Wxation; speciWcally Kastner and colleagues (Kastner et al. 1998, 1999, 2001) Wnd that evoked signal diVerences between items presented sequentially and simultaneously in the upper-right visual Weld are smaller when attention is directed to one of those items rather than to a stream of items at Wxation. If, on the other hand, we Wnd that diVerence between sequential and simultaneous presentation conditions remains equivalently large even when attention is directed to the Wve items; we would conclude that attention cannot reduce suppressive interactions among multiple stimuli to which it is simultaneously
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applied. In this case, suppression indices for unattended and attended conditions should be roughly equivalent. Note that, in this paradigm, it is possible for attention to produce an enhancement (main eVect of attention) without modulating suppressive interactions (interaction of attention and presentation conditions) or vice versa.
Materials and methods Subjects: We tested 8 volunteers (5 males; ages 24–36), all with normal or corrected to normal visual acuity. Because our paradigm is so similar to that with which Kastner et al. (1998) demonstrated an interaction between attention and presentation method, we used the data reported by Kastner et al. (1998) to estimate the number of participants needed to detect such an interaction in V4 signal. These calculations revealed that data from four participants would be required to detect an interaction of comparable size and consistency with a statistical power of 98% (Lenth 2007). To further decrease the likelihood that low power was responsible for any lack of interactions between attention and presentation method in V4 activity we observed, we doubled this number to 8 volunteers. Participants gave written informed consent to participate in this study, which was approved by the Institutional Review Board of the University of Illinois at Urbana Champaign and were paid for their participation. Stimuli: Four shapes (hearts, squares, circles, or triangles) were crossed with six colors (red, blue, yellow, green, orange, or purple) and four textures (solid, horizontal stripes, vertical stripes, and diagonal stripes) to create 96 diVerent stimuli. We centered a stimulus in each of Wve squares arranged in a grid (gray on a black background) that was present throughout the experiment in the upperright visual Weld (see Fig. 1). Five 2-sided squares comprised this grid. The two uppermost squares were centered 5.25° from the horizontal meridian and 1.11° and 3.18° from the vertical meridian, respectively. The two central most squares were centered 3.18° from the horizontal meridian and 3.18° and 5.25° from the vertical meridian, respectively. The lowermost square was centered 1.11° above the horizontal meridian and 5.25° from the vertical meridian. The center most item of this display was position 4.5° of visual angle from Wxation; this distance is intermediate between those used by other studies (Bles et al. 2006: 2.5°; Kastner et al. 2001: 5.5°) that have shown that directing attention to an item, rather than to an item at Wxation, modulates the competitive interactions of that item with its neighbors. The Wve stimuli appeared either sequentially (low potential for suppressive interactions) or simultaneously (high potential for suppressive interactions). During sequential presentation, each of the Wve stimuli appeared in isolation
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Fig. 1 Experimental design and stimuli (a, b, c, d). Five color/ shape/texture conjunctions appeared in the periphery of the upper-right quadrant. All Wve items appeared either (a) sequentially or (b) simultaneously within a period of 1.25 s. Participants monitored either (c) a stream of characters and symbols at Wxation for the letter a or (d) Wve locations in the upper-right visual Weld for an infrequent predeWned conjunction of color, spatial frequency, and line orientation
(in a random order) for 250 ms (see Fig. 1a). When presented simultaneously, the Wve patches appeared together for 250 ms (see Fig. 1b). Onset times for the simultaneous items jittered such that the average stimulus onset asynchrony (SOA) was 1.25 s (range, 750 ms–1.75 s). In both conditions, each stimulus appeared for 250 ms, and each square in the grid was Wlled once and only once every 1.25 s on average. Total visual stimulation at each location was therefore equated in the two conditions. Although we acknowledge that his manipulation does assume that the integration of neural activity evoked by stimuli presented over an extended period of time does not introduce nonlinearities between neural and hemodynamic measures, this assumption is consistent with current data regarding this issue (Boynton et al. 1996). Throughout the fMRI experiment, participants viewed a rapid serial visual presentation (RSVP) stream at Wxation. This was a 4 Hz stream of digits (1–9) and ASCII symbols (%, &, *, #) and a single letter (“a”), all presented in a white 30 pt font. We note that this stream did not extend beyond Wxation by more than .5° in any direction, and thus the receptive Weld size of the majority of V4 cells stimulated by these items would be unlikely to extend more that one degree of visual angle (Motter 2009) and would be equally distributed among right and left and ventral and dorsal V4. The representations of items presented at Wxation would
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consequently be unlikely to interact competitively with upper-right visual Weld items with an eccentricity of 4.5° of visual angle (represented primarily by right ventral V4). This RSVP stream was present throughout the run, with the exception of a 2 s period before and after each visual stimulation block. This period was used in attend-Wve runs to cue participants to move their attention to or from the peripheral presentation grid. It was included in attend-Wxation runs to maintain the greatest possible similarity between the two conditions. Vision Egg stimulus presentation software (Straw 2008) running under Windows XP Professional (Microsoft Corp) on a Pentium 4 Dell PC controlled stimulus presentation. Participants viewed the stimuli on a back projection system run through a Proxima C410 digital projector (InFocus Corp). fMRI task and trial structure: We asked participants to attend either to the RSVP stream throughout the run or to the colored items when they were present and the RSVP stream when they were absent. While attending to the RSVP stream (attend Wxation), participants searched for a lower case “a” (see Fig. 1c). While attending to the shape stimuli (attend Wve), participants searched the stimuli for one of two conjunctions of color, shape, and texture, randomly selected from the sets of colors, shapes, and texture combinations described above (See Fig. 1d). The targets
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changed every four runs. They appeared at the beginning of each “attend-Wve” run, alternating at a rate of 1 Hz, to help participants remember them. The attention condition (attend Wve or attend Wxation) remained constant through each run and occurred in one of two four-run sequences (AFix-A5-A5-AFix or A5-AFix-AFix-A5), randomly chosen every four runs. As an aid to our participants’ memories, we placed a red digit (40 pt font), present throughout the run, 2° below Wxation to indicate the attention condition: “0” during the attend-Wxation condition and “5” during the attend-Wve condition. We considered each 1.25 s period in which all Wve grid squares were stimulated a “trial”. Because we were interested in the inXuence of a sustained cognitive state (topdown, spatial attention) on evoked signal in visual cortex rather than the inXuence of speciWc stimulus characteristics on the actions of the attentional system, we were able to take advantage of the increased statistical power and BOLD signal change available in a “blocked” fMRI design (see Amaro and Barker 2006 for a review of this issue). Each 290-s run consisted of eight 20-s blocks (16 trials) of either sequential or simultaneous presentations interleaved with 10-s blank periods. In addition, each run began and ended with a 10-s blank periods. The order of sequential and simultaneous blocks (SEQ-SEQ-SIM-SIM-SIM-SIM-SEQSEQ or SIM-SIM-SEQ-SEQ-SEQ-SEQ-SIM-SIM) randomly varied on each run. Each participant completed 8 runs. Shape targets occurred once in each location in each condition in each run (for a total of 10 targets per run). In order to prevent participants from anticipating the number of targets in each block, we jittered target presentation such that one block from each presentation condition contained zero targets, one block from each presentation condition contained one target, and two blocks from each presentation condition contained two targets. In order to encourage participants to attend to all Wve locations in the upper-right visual Weld during attend-Wve runs, we forced the non-target stimuli that occurred in each of the locations to contain one of the three target-deWning features on all trials. During the attend-Wxation runs, all stimuli in the upper-right visual Weld contained the same target-deWning features from an “attend-shape” run that was not temporally adjacent to the current run. This ensured that we were sampling from the same cell populations across attend-Wve and attend-Wxation runs but reduced the likelihood that subjects would notice the manipulation. In all conditions, participants maintained Wxation on the RSVP stream and indicated the presence of a task relevant target by pressing a button with their right index Wnger. Responses were collected using a USB optically isolated 10-button response boxes (Rowland Institute, Harvard).
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Eye-movement monitoring: During fMRI scanning, eye movements from all participants were monitored using a View Point eye-tracker (Arrington Research, Inc). Training: Participants in both experiments also completed eight runs of training trials the day before undergoing fMRI scanning. We trained participants to maintain Wxation on the RSVP stream throughout the blank and visual presentation blocks by monitoring their eye movements and providing feedback whenever their gaze deviated from Wxation by more than 1° of visual angle for more than 150 ms. Feedback was a 512 Hz 80 db tone that persisted until participants returned their gaze to Wxation. In order to help participants remain engaged during training, we decreased the duration of the “blank” periods to 5 s. Stimuli were presented using Vision Egg (Straw 2008) software running under Windows 2000 (Microsoft Corp) running on a Pentium 4 Dell PC. Eye movements were monitored using a head-mounted Eye-Link II tracker. In all other ways, we held training conditions identical to those described for fMRI testing. Data acquisition and analysis: Imaging data were acquired in a 3-T head-only scanner (Allegra, Siemens) using a standard head coil. We acquired EPIs (TR = 2 s; TE = 20 ms; Xip angle = 90°; Weld of view = 160 £ 160 mm; voxel size = 2.5 £ 2.5 £ 3 mm, no gap) in 20 ascending coronal slices starting at the posterior pole. We collected 8 experimental runs of 145 repetitions. To assist in registering EPI images to anatomic space, we collected T2-weighted anatomical images (TR = 9,100 ms; TE = 96 ms; Xip angle = 150°; 128 £ 128 matrix) with 49 coronal slices aligned at the posterior pole to EPI slices from the same session. For all participants tested, we collected multiple high-resolution T1 anatomic images collecting during retinotopy scanning (see Scalf and Beck 2010 for retinotopic mapping procedures), to which we registered our EPI images. We used tools from the fMRIB Software Library (FSL) to analyze our functional data. Data were motioned corrected using McFLIRT (FSL 3.3: Smith et al. 2004; Jenkinson et al. 2002) We used FEAT (FMRI Expert Analysis Tool) v 5.2 to submit functional data from individual runs to multiple regression analysis. Prior to analysis, data were subjected to slice-time correction, mean-based intensity normalization, and to highpass temporal Wltering (sigma = 15 s) and pre-whitened to correct for local autocorrelation (Woolrich et al. 2001). We modeled two regressors of interest (sequential and simultaneous presentation) in the analysis of each run. These square-waves were convolved with a gamma model of the HRF (phase, 0; st dev, 3 s; mean lag, 6 s). Although targets were unevenly distributed throughout these blocks of stimulation (and thus unlikely to produce activation that was well “Wt” by the sequential and simultaneous block regres-
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sors), we further reduced the likelihood that our regressors of interest reXected activation associated with attention “collapsing” around a target shape stimulus by including a single event-related regressor of upper-right Weld targets. We convolved these events with a double-gamma model of the HRF (Phase 0 s), which in our previous work better captured the extrastriate activity associated with brief events than does the single-gamma model that we typically use to model block eVects (Scalf and Beck 2010). No other regressors were included in statistical modeling. These parameter estimate maps were registered into the participant’s individual anatomic space and into standard space using FLIRT (Jenkinson et al. 2002). The data reported in the Wgures and results section correspond to average parameter estimates of sequential and simultaneous regressors extracted from regions of interest in V4 (see below).
MPRAGE space). Because the edges of the diVerently resolved MPRAGE and EPI voxels are not in direct correspondence, the number of EPI voxels sampled by Featquery will vary both as a function of the size of the region activated by the ROI identiWcation process, the degree of correspondence between EPI and MPRAGE edges in that ROI in that participant, and the interpolation threshold set by the experimenter. We allowed Featquery interpolation thresholds to vary from .2 to .5; such that signal from no more than 45 and no fewer than 30 voxels in functional space (3 £ 3 £ 3 mm) was included in the averaged parameter estimates from each run. An interpolation threshold of .3 or less failed to produce an acceptable number of voxels only in a single participant’s ROI, whose threshold was set at .5.
Region of interest analysis procedures
To determine whether any regions outside of occipital cortex were sensitive to our manipulations, we submitted the lower-level parameter estimates described above to partialhead analysis. For each participant, parameters estimate maps from each run were transformed into standard space and subjected to higher-level, Wxed-eVects analysis in FEAT (Woolrich et al. 2001). For each participant, this analysis produced one parameter estimate map for each of the four conditions of interest (attend-Wxation simultaneous, attend-Wxation sequential, attend-Wve simultaneous, and attend-Wve sequential) as well as a contrast parameter estimate map for each contrast of interest (attend Wve vs. attend Wxation; sequential vs. simultaneous, attention X presentation conditions interaction). For each contrast of interest, the relevant contrast map from each participant was submitted to a group-level, mixed-eVects analysis (FLAME, Beckmann et al. 2003; Woolrich et al. 2004). Images were thresholded using clusters determined by ¡2.3 > Z > 2.3 and a corrected cluster signiWcance threshold of P = .01 (Worsley et al. 1992).
In order to compare activity for the same physical stimulus under diVerent attentional conditions, we used data from a separate retinotopic mapping session to identify regions of interest (ROIs) in V1 through V4 that represented the Wve locations in the upper-right visual Weld. Although we identiWed ROIs in each visual area, we were primarily interested in results from V4 because previous studies using stimulus parameters similar to ours showed the largest eVects of both suppression and attention in V4 (Kastner et al. 1998, 2001); regions V1, V2, and VP typically do not show signiWcant eVects of attention with similar displays (Kastner et al. 2001; Bles et al. 2006). To identify the ROIs, we concatenated all EPI runs into a single data set, which was motion corrected (Jenkinson et al. 2002), slice-time corrected, mean base intensity normalized, and high-pass temporal Wltered (sigma = 15 s). These data were pre-whitened to correct for temporal serial auto-correlation and subjected to multiple regression analysis (FEAT; Woolrich et al. 2001). We modeled the occurrence of upper-right Weld items (as opposed the blank periods) as our regressor of interest. The resulting statistical maps were sampled into Xatmap space created by Freesurfer, which we used to select any superthreshold voxels (Z > 2.5) that fell within each visual area and to project the masks drawn for each participant back to their individual high-resolution anatomic space. We used Featquery (Smith et al. 2004) to extract the parameter estimates associated with the sequential and simultaneous regressors from the main analysis in the ROI’s identiWed in each individual from each run. For each participant, we computed the average parameter estimate for each experimentally relevant condition for each ROI. Featquery applied the MPRAGE to EPI transformation matrix calculated during image registration to determine which EPI voxels fell within the ROI (selected in
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Whole-volume analysis procedures
Results Region of interest analysis Analysis of the BOLD signal extracted from each participant’s V4 ROI revealed a main eVect of presentation method (F(1,7) = 32.96; P = .0007); consistent with previous data (Scalf and Beck 2010; Kastner et al. 1998, 2001; Beck and Kastner 2005, 2007), sequential presentations evoked signiWcantly greater activity than simultaneous presentations (Fig. 2). This is in accordance with predictions that simultaneously presented stimuli suppress one another’s representations in V4. We also found a main eVect of attention (F(1,7) = 6.248; P = .041); V4 signal was
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Fig. 2 Activation (parameter estimates/beta weights) in V4 for each of the four conditions. V4 showed a main eVect of presentation condition; sequential presentation evoked more activation than did simultaneous presentation. We also found a main eVect of attention; the Wve items in the upper-right quadrant evoked more signal when attention was directed toward them rather than to the RSVP stream at Wxation. Importantly, we found no interaction between these factors; directing attention to multiple items did not inXuence their suppressive interactions
higher when locations in the upper-right visual Weld were attended (attend-Wve) than when they were not (attend Wxation). Importantly, however, we found no evidence of an interaction between these factors (F(1,7) = .05; P = .823). The diVerence between the signal evoked by the peripheral items under sequential and simultaneous presentation conditions was unaVected by whether or not attention was directed to them. As in previous studies (Scalf and Beck 2010; Kastner et al. 1998, 2001; Beck and Kastner 2005, 2007), we also examined suppression indices [(Sequential¡Simultaneous)/(Sequential + Simultaneous)], which quantify the diVerence between sequential and simultaneous presentation conditions in a baseline-independent manner, to further assess whether attention modulated competitive interactions among the items. A paired t-test indicated that suppressive interactions among the items were equally high when they were attended (.14) or unattended (.14) (t(7) = .08; P = .94) (see Fig. 3). Finally, it is important to note that this lack of interaction was obtained in the face of clearly signiWcant eVects of both attention and presentation condition as well as with a number of participants that exceeded that which was indicated by power calculations based on a previously obtained interaction of attention and presentation condition, in which only a single item was attended (Kastner et al. 1998). Analysis of ROIs extracted from area VP reXected a main eVect of presentation method (F(1,7) = 29.63; P = .001); sequentially presented stimuli evoked more signal than did simultaneously presented stimuli. Analysis of
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Fig. 3 Stimulus suppression indices [SSIs: (sequential ¡ simultaneous)/ (sequential + simultaneous)] in V4 for each attentional condition. SSIs were insensitive to whether Wxation or the Wve items were attended
Fig. 4 Stimulus suppression indices [SSIs: (sequential ¡ simultaneous)/ (sequential + simultaneous)] for areas V1, V2 and VP. As seen previously, SSIs increased with increasing visual area
suppression indices (mean = .14) conWrmed that they were signiWcantly greater than 0 (t(7) = 6.4; P = .0004) (see Fig. 4). No other main eVects or interactions were signiWcant (P > .13), including the main eVect of attention. As mentioned earlier, however, attention eVects are typically much weaker in visual areas that precede V4. Analysis of ROIs extracted from area V2 reXected a main eVect of presentation method (F(1,7) = 6.84; P = .001); sequentially presented stimuli evoked more signal than did simultaneously presented stimuli. Analysis of suppression indices (mean = .07) conWrmed that they were signiWcantly greater than 0 (t(7) = 2.61; P = .035) (see Fig. 4). No other main eVects or interactions were signiWcant (P > .13).
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Analysis of ROIs extracted from V1 showed no main eVects or interactions (P > .24). Suppression indices (mean = .02), in V1, did not diVer signiWcantly from 0 (t(7) = .59; P = .574) (see Fig. 4). Whole-volume analysis results We used group analysis to look for eVects of attentional condition, presentation condition, and their interactions in regions outside of occipital cortex. Under conditions in which items were present in the upper-right visual Weld, directing attention to them rather than to the RSVP stream at Wxation produced clusters of signiWcant activation in left superior parietal lobule (BA 7: peak Z = 3.54; x = ¡32, y = ¡69, z = 55, k = 140, p of k = 5.96e-08), right superior parietal lobule (BA 7: peak Z = 3.7; x = 32, y = ¡60, z = 60, k = 73, p of k = 1.47e-04), and right fusiform gyrus (BA 19 : peak Z = 3.46; x = ¡24, y = ¡66, z = ¡8; k = 105; p of k = 2.26e-06). Directing attention to the RSVP stream at Wxation rather than the items in the upper-right visual Weld produced signiWcant activation in precuneus (BA 7; peak Z = 3.15; x = 2, y = ¡60, z = 40; k = 62; p of k = 7.04e-4) and the right middle temporal gyrus (BA = 39; peak Z = 3.33, x = ¡58, y = ¡65, z = 25; k = 89; p of k = 1.72e-05). SigniWcant clusters of activation did not emerge in the contrast between presentation method (sequential vs. simultaneous) or its interaction with attentional condition. Behavioral results Reaction times1 and sensitivity measures (d-prime) to the targets in the attend-Wve condition indicated that although participants were fairly slow to detect targets [1,092 ms for sequential (SD = 130 ms, acc = 63%), 1,107 ms for simultaneous (SD = 64 ms, acc = 66%)], they were nonetheless fairly sensitive to their presence for both sequential (d⬘ = 2.61) and simultaneous (d⬘ = 2.76) presentations. Neither the RTs nor d-prime measures showed any diVerences between sequential and simultaneous condition, t(7) = 0.29, P = 0.78 and t(7) = 0.77, P = 0.46, respectively. We note, however, that because our main goal in this experiment was to assess the eVects of attention when distributed across all Wve locations, the number of target trials was kept purposefully low. This low number of targets and the blocked nature of our trial design were not optimal for detecting behavioral diVerences among conditions. If it is true that attention applied to multiple items is unable to reduce their competitive interactions, however, 1 Reaction time for both sequential and simultaneous presentation conditions was calculated as the time between the appearance of the taskrelevant target item and the execution of a response.
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this should have behavioral consequences such that multiply attended simultaneously presented (competing) items are more diYcult to process than are multiply attended sequentially presented (non-competing) items. Because the experimental design in the scanner was not optimized to detect such behavioral diVerence (i.e., targets were presented on only 20% of trials), we addressed this issue by testing nine participants outside the fMRI environment in a modiWed version of the experiment presented in the scanner. Stimulus presentation, response collection, and eyemovement monitoring were controlled using the system, described above, used for behavioral training. The spatial layout and components of the stimulus display were identical to those described above. In this experiment, however, participants saw no RSVP stream at Wxation and attended only to items presented in the Wve-item grid. In each trial, participants Wxated on a small dot placed at the center of the screen. After optical drift correction was completed by the eye-tracker, this dot changed to a Wxation cross. Participants remained Wxated on that cross and monitored the grid in the upper-right visual Weld for color/shape/texture conjunction speciWed at the beginning of each block. Participants indicated responses via a keypad; they were instructed to respond as quickly as possible with their right index Wnger if the conjunction appeared at any point in the display and were instructed to respond with their right middle Wnger if they did not see the target at any point in the trial. Drift correction for the next trial began only after the participant responded. Participants were instructed to hold their eye still throughout the trial and told that they would have to repeat at the end of the block any trials on which the had moved their eyes more than 1° of visual angle from Wxation for more than 150 ms. Such movements were signaled to the participants by a loud buzz. At the beginning of each block, new color/shape/texture conjunction was randomly selected and presented to the participant. A sequence of 100 trials was constructed. In this sequence, the levels of the factors presentation method (sequential, simultaneous), target (present, absent), target location (squares 1–5), and target timing (patches 1–5; this factor did not aVect simultaneously presented trials) were fully crossed and equiprobable. The order of these trials was then randomized. During the practice block, participants were presented with only 20 of these trials; during the three test blocks, participants were presented with all 100 trials. If participants moved their eyes during any trial, a repetition of that trial was appended to the end of the block. The test blocks ended when the participants had performed each of the 100 trials types without moving their eyes from Wxation. All participants completed testing in under an hour. We observed clear diVerences in performance under sequential and simultaneously presentation conditions in
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this paradigm. Sensitivity was signiWcantly (t(8) = 2.67; P = .03) greater under sequential presentation conditions (d⬘ = 3.44) than under simultaneous presentation conditions (d⬘ = 2.89). We also calculated reaction time data for target present trials (for the sequential presentation condition, we included only those trials for which the target was the last in the sequence). Reaction time data were not collected from two subjects because of a programming error; the remaining seven participants, however, showed signiWcantly (t(6) = 10.45; P = .000045) faster responses to targets presented under sequential conditions (763 ms, acc = .87) than to those presented under simultaneous presentation conditions (892 ms, acc = .84). fMRI eye-movement results We counted any Wxation that persisted for 165 ms (5 samples) or longer at a distance greater than 1.5° of visual angle as a deviation from Wxation. We then calculated the percentage of trials in which a deviation had occurred into each of the four quadrants of the visual Weld (upper left, upper right, lower left, and lower right). We note that within any given trial (which lasted 1.25 s), deviations could occur in more that one quadrant. We subjected these data to a repeated measures ANOVA, using the factors attention (attend Wxation, attend display), presentation (sequential, simultaneous), and quadrant (upper left, upper right, lower left, and lower right. We found a main eVect of quadrant [F(3,21) = 4.01; P = .02]; participants tended to deviate (on 12% of trials) to the upper-right quadrant of the visual Weld (the one containing the stimulus grid centered 4.5° of visual angle from Wxation) more than to the other quadrants; pairwise comparisons indicate that this was marginally more than occurred for the upper left quadrant (mean = 3%, P = .07) and marginally more that occurred for the lower right quadrant (mean = 2%; P = .05). Deviations into the lower left quadrant (mean = 4%) were not diVerent from those into other quadrants (P = .12). We also found a signiWcant interaction between the factors attention and presentation; quadrants were “visited” on a higher percentage of trials if attention was directed to Wxation under simultaneous presentation conditions (7% of trials) than under other conditions (5% of trials). We note that this interaction opposes the Wndings of our imaging ROI analysis and so do not compromise the interpretation of our data. SpeciWcally, increases in the number of deviations from Wxation under attend Wxation, simultaneous presentation condition should weaken the BOLD signal evoked in the ROI relative to those obtained in other conditions. This weakening, in turn, should have lead to a larger diVerence between sequential and simultaneous presentation conditions (and consequently, greater suppression indices) for the attend-Wxation condition than the attend-display condi-
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tion. Despite this opportunity for eye movements to increase the likelihood that directing attention to Wxation instead of the display would increase our BOLD measures of inter-item suppression, we found no such eVects. No other main eVects or interactions were present in the eyemovement data (P > .10).
Discussion In this experiment, we manipulated the attentional status and potential for suppressive interactions among a group of visual items to investigate Wrst, whether attention to multiple items modulated suppressive interactions among those items at all, and second, whether attention continued to increase evoked extrastriate signal under conditions in which it was likely to have little eVect on inter-item suppressive eVects. Sequential presentation evoked greater activation in V4 than did simultaneous presentation, indicating that items did interact in a mutually suppressive manner when presented simultaneously. This diVerence was unaVected by the attentional status of the items, however, indicating that attention was unable to modulate that suppression. Similarly, suppression indices were equivalent whether or not participants were attending to the peripheral items. Despite its failure to modulate suppressive interactions, directing attention to the items nonetheless signiWcantly increased the activation evoked by the attended items. It appears, then, that attention can be eVectively allocated to enhance the BOLD signal of multiple, mutually inhibitory representations, even if it has no inXuence on their suppressive interactions. Our whole-volume analysis of parietal and posterior temporal activation conWrmed that participants’ attentional systems responded appropriately to the instructions to monitor multiple items. Consistent with other Wndings in the literature, directing attention to multiple items increased activation in the superior parietal lobule bilaterally (Scalf and Beck 2010; Xu and Chun, 2009; Mitchell and Cusack 2008). Interestingly, areas in the precuneus and the middle temporal gyrus that are often implicated in the “default mode network” (Greicius and Menon 2004; Fox and Raichle 2007; Weissman et al. 2006) showed signiWcant activation as a result of directing attention to the single RSVP stream at Wxation rather than the items in the upper-right visual Weld. Our behavioral data indicate that attending to multiple items was more diYcult than attending to the RSVP stream at Wxation; it may be that our data reXect a replication of the Wnding that the default mode network deactivates with increasing task demand (e.g., Singh and Fawcett 2008; Mason et al. 2007). Alternatively, relative increases in activity in the “default mode network” and relative decreases in activity in the “dorsal attention network”
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(which included superior parietal regions) may reXect a shift away from high demands placed on spatial selective attention (Sadaghiani et al. 2009); in our paradigms, demands on spatial selective attention should certainly have been higher when attention was decoupled from Wxation and directed to the items in the upper-right visual Weld than when it was directed to the RSVP stream at Wxation. Taken together, the results from our analysis of task-related changes in parietal and prefrontal activation conWrm that our manipulations of task demand appropriately and eVectively activated regions associated with spatial selective attention. Our data are the Wrst, to our knowledge, to explicitly decouple attention-related signal enhancement from the modulation of inter-item suppression. Previous work directly investigating the relationship of attentional modulation to inter-item suppression has shown that the more vulnerable task-relevant stimuli are to stimulus suppression, the greater the signal enhancement they derive from attention (Kastner et al. 1998, 2001; Bles et al. 2006; Reynolds and Desimone 2003; Reynolds et al. 1999). These data have suggested that the enhancing eVects of attention are closely linked to the modulation of inter-item suppressive eVects. Our data demonstrate that this is not necessarily the case; attention can increase signal evoked by the attended items while leaving them vulnerable to the same suppressive interactions that are at play when the same items are unattended. The strictest claims of the bias competition model, namely that attention-related enhancement necessarily reXects only the resolution of inter-item suppression (Desimone 1996; Duncan et al. 1997), are already inconsistent with numerous studies reporting attentionrelated enhancement of the representations of stimuli whose spatial and temporal placement protect them from suppressive interactions (e.g., Pinsk et al. 2004; McMains et al. 2007; Sylvester et al. 2009; McMains and Somers 2004, 2005). These data can be accommodated, however, within a more moderate interpretation of biased competition theory that posits that attention-related enhancement primarily reXects the potential of top-down biasing to resolve suppressive interactions should they exist. Our data, in contrast, demonstrate that attention-related enhancement can be observed not only when it need not but also when it cannot resolve inter-item suppression. Top-down attention, then, must reXect more than the resolution or potential resolution of inter-item suppression. Our data are consistent with predictions that may be extrapolated both from out previous work (Scalf and Beck 2010) and from the biased competition model; namely, that when attention is applied to multiple competing items, it should be prevented from resolving those competitive interactions by its inability to bias them in favor of a single item. The data reported here indicate that attention is relatively
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unable to modulate suppressive interactions among items to which it is directed simultaneously. When we consider our current Wndings in conjunction with our previous Wndings, we conclude that although attention is able to eVectively enhance the representations of multiply attended items, it can only exert its full eVect on the representations of singly attended items (Scalf and Beck 2010) because only under that latter conditions, it can resolve competition for representation. Our Wndings conWrm that attention directed to multiple items does enhance the response evoked by them. Since our data also indicate that this enhancement cannot reXect reductions in suppressive inXuences among those items, it must have some other cause. Feature-based attention may be one such possibility. In this experiment, we compared conditions in which participants searched for a speciWc conjunction of color, shape, and texture to those in which the monitored Wxation from a speciWc letter. We also presented target-deWning features in every location on every trial of the attend-Wve condition; such conditions have been shown to produce non-spatially speciWc enhancement of feature evoked activity (Bichot et al. 2005). There are several alternative explanations of the attentional enhancement we observed. These may reXect tonic baseline biasing eVects (Kastner et al. 1999; Buracas and Boynton 2007; Sylvester et al. 2009; Luck et al. 1997), ampliWcation, or gain control, of evoked signal (Luck et al. 1997; Mangun et al. 1993), or noise reduction (Lu and Dosher 1998); notice, however, that all of these alternatives to features based attention are spatially speciWc mechanisms. In our current experiment, changes in the location and features that required attention were completely confounded; it is therefore not possible for us to determine to what extent featural and spatial attention contribute to the attentional enhancement we observe in the current data. In our previous data (Scalf and Beck 2010), however, we varied the spatial location of the attended information while holding constant the demands placed on featural attention. Under these conditions, we found no evidence that directing attention to multiple competing items enhanced the signal they evoked (we found typical attentional enhancement of the signal evoked by multiple noncompeting items). When we consider the two studies together, then, we suspect that multiple competing items are more likely to beneWt from feature-based mechanisms of attention than from space-based mechanisms of attention. Future research will be required to more fully investigate this issue. Regardless of the source of this enhancement, it is clear that the ability to enhance and the ability to modulate suppressive interaction can be dissociated. The increased BOLD signal we observed for attended items presumably reXects a higher Wring rate for the neurons representing those items. That higher Wring rate, however, does not come
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at the expense of the surrounding items because attention is also directed to the surrounding items and boosts their Wring rate to an equivalent extent. In other words, all the neurons representing the attended items may be Wring more vigorously than when they are unattended, but as long as attention is directed to all the items equally, no single item will have a Wring rate greater than the rest, and thus no single item will be signaled more clearly than the rest. These results suggest that models of attention may gain further traction if they are extended beyond the various eVects of attending to a single item (Desimone and Duncan 1995; Reynolds and Heeger 2009) to situations in which attention is directed to multiple items simultaneously. Acknowledgments We would like to thank Walter Boot, Eamon Caddigan, and Mathew Hall for assistance in eye tracking and Holly Tracey and Nancy Dodge for assistance with data collection. This work was funded by NIMH grant R03 MH082012 (DMB).
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