Cognitive Brain Research 22 (2005) 333 – 348 www.elsevier.com/locate/cogbrainres
Research report
Spatio-temporal dynamics of top-down control: directing attention to location and/or color as revealed by ERPs and source modeling Heleen A. Slagtera,*, Albert Koka, Nisan Molb, J. Leon Kenemansb a
Department of Psychonomics, University of Amsterdam, Roeterstraat 15, 1018 W.B. Amsterdam, The Netherlands b Departments of Psychonomics and Psychopharmacology, Utrecht University, The Netherlands Accepted 8 September 2004 Available online 18 October 2004
Abstract This study investigated the nature and dynamics of the top-down control mechanisms that afford attentional selection using event-related potentials (ERPs) and dipole-source modeling. Subjects performed a task in which they were cued to direct attention to color, location, a conjunction of color and location or no specific feature on a trial-by-trial basis. Overall, similar ERP patterns were observed for directing attention to color and location, suggesting that spatial and non-spatial attention rely to a great extent on similar control mechanisms. The earliest attention-directing effect, at 340 ms, was localized to ventral posterior cortex and may reflect processes by which the cue is linked to its associated feature. Only late in the cue-target interval, differences in ERP were observed between directing attention to color and location. These originated from anterior and ventral posterior areas and may represent differences in, respectively, maintenance and perceptual biasing processes. The ventral posterior sources estimated for these late effects of directing attention to location and color were located posterior to those estimated for the modulatory effects of, respectively, spatial and non-spatial attention. This suggests that the precise neural populations involved in perceptual biasing and attentional modulation may differ. Conjunction cues initially elicited less posterior positivity than color and location cues, but evoked greater central positivity from 540 ms on. This central effect may reflect feature integration or ongoing processes related to cue-symbol translation. These results extend our understanding of the spatio-temporal dynamics of top-down attentional control. D 2004 Elsevier B.V. All rights reserved. Theme: Neural basis of behavior Topic: Cognition Keywords: Spatial; Non-spatial; Attentional control; Attentional selection; Event-related potentials; Dipole modeling
1. Introduction Functional neuroimaging studies have shown that stimuli presented at attended positions in space (e.g., Ref. [18]) or with an attended non-spatial stimulus feature, such as color (e.g., Ref. [5]), elicit enhanced activation in sensory brain areas corresponding to the attended stimulus dimension. This attention-related sensory facilitation of target processing enables us to respond faster and more accurately to important external events. Advance knowledge of both spatial and non-spatial stimulus characteristics has been * Corresponding author. Fax: +31 20 6391656. E-mail address:
[email protected] (H.A. Slagter). 0926-6410/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.cogbrainres.2004.09.005
shown to improve behavior [29,30]. Nevertheless, results from event-related potential (ERP) studies indicate that the temporal dynamics of the neural mechanisms underlying attentional modulation of target processing differ between spatial and non-spatial attention. Whereas visuospatial attention results in enhanced amplitudes of the exogenous components P1 and N1 evident in the ERP to stimuli at both attended and unattended locations as early as 80–90 ms post-stimulus (e.g., Refs. [8,41]), selection based on nonspatial visual stimulus features, such as color or form, is reflected by effects starting at around 150 ms post-stimulus, which are super imposed on the evoked components and have a very different morphology (e.g., Refs. [16,20]). Thus, results from ERP studies indicate that modulation
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effects are not only of longer latency when attention is directed to a non-spatial stimulus feature, but they are also qualitatively different for spatial and non-spatial attention. Given these dissociations observed with ERP, one may ask whether the control processes that direct the focus of attention and may produce attentional modulation of sensory responses differ between spatial and non-spatial attention. Only fairly recently, research has turned to address this question (for review, see Refs. [46,64] ). A straightforward way to investigate attentional control processes is to examine brain activity in the period before the test stimulus is presented, that is, when subjects direct their attention to a relevant stimulus feature in response to an attentiondirecting cue. Recent studies using functional magnetic resonance imaging (fMRI) have revealed a network of activated brain areas in the period between attentiondirecting cue and test stimulus, encompassing both frontal and parietal regions for spatial [6,22,25,26,60] as well as non-spatial [37,48,49,58] attention. However, some domainspecificity appears to be present within this network, with dorsal frontal and parietal areas and ventral occipitotemporal regions being more strongly activated by, respectively, spatial and non-spatial attention-directing cues [13,50]. In addition, several studies have observed increased activation in visual areas not only in response to target stimuli, but also in the period preceding the presentation of the target stimulus (e.g., Refs. [13,22,26]). The common interpretation of these findings is that higher order areas in frontal and parietal cortex send biasing signals to functionally specialized sensory areas, so that they in turn can selectively process target information [7]. Although fMRI provides detailed information about the localization of neural processes, its temporal resolution is still in the order of hundreds of milliseconds to a few seconds at best [44]. This is much longer than the time it takes to fully direct attention [39]. The high temporal resolution of the event-related potential technique makes it an excellent tool for the study of control processes and preparatory states, as it can relate specific differences in brain activation to changes in specific stages of information processing. This temporal information is essential for a full understanding of the attentional control mechanisms reflected in fMRI activations. Even though fMRI studies have shown involvement of roughly the same network of brain regions in the directing of attention to spatial and nonspatial stimulus attributes [13,50], the temporal sequence of activation within these regions may be dependent on the nature of the to-be-attended stimulus material. Several ERP studies have previously investigated the directing of attention to a location in space [9–11,15, 17,40,47,61,62] and non-spatial features [28,63]. However, a comparison between results from these studies is at present restrained by the fact that most studies of spatial attentional control subtracted ERP responses to cues directing attention to the left from ERP responses to cues directing attention to the right hemifield [9–11,17,21,47,61,62] (but see Refs.
[15,40]). This comparison has revealed a sequence of effects related to directing attention to a specific location in space, consisting of an early directing attention negativity (EDAN) at posterior parieto-occipital electrodes between 200 and 400 ms post-cue, an anterior directing attention negativity (ADAN) at frontal electrodes between 300 and 500 ms post-cue, and a late directing attention positivity (LDAP) over lateral ventral occipito-temporal scalp regions starting at around 500 ms post-cue. Yet, these effects cannot easily be compared to results from studies of non-spatial attentional control in which such an attend-left versus attend-right comparison is obviously not possible. In addition, one may ask whether these cue-direction-related effects reflect the full temporal pattern of spatial attentional control (see also Ref. [57]). Several studies of spatial top-down control have reported behavioral cueing effects and attentional modulation effects (i.e., P1, N1) in the absence of these cue-directionrelated ERP effects (i.e., EDAN [10,11], ADAN [15] and LDAP [40,47]). This suggests that some attentional control processes that may be mandatory for the establishment of an attentional bias are not lateralized and, thus, do not show up in the left–right subtraction. This further complicates an integrative interpretation of the results from ERP studies of spatial and non-spatial top-down control. Thus, in order to adequately isolate the complete pattern of spatial or nonspatial attentional control, one needs to compare the attention-directing condition with a reference condition that controls for processes that are not specific to the actual initiation and directing of attention, such as cue-identification and motor preparation processes, but that does not call upon attentional control mechanisms. In the present study, we examined the extent to which topdown control processes are stimulus material-unspecific (i.e., general) or depend on the nature of the to-be-attended stimulus feature (i.e., domain-specific) using a within-subject design and a reference cue condition. ERPs elicited by location and color attention-directing cues were compared to ERPs elicited by reference cues to isolate processes related to directing attention to location and color. The underlying neural source configurations of the observed spatial and nonspatial attention-directing effects were compared against each other to reveal possible differences in the configuration and/ or timing of activated brain areas. Based upon positionspecial models of attention [31,33,34,53,55,56], it can be hypothesized that pre-target biasing effects of spatial attention result from an initial activation in dorsal posterior areas, which maintain location representations, which is followed in time by activation in ventral posterior areas, which maintain spatially corresponding feature representations. Biasing effects of non-spatial attention, on the other hand, would be reflected by a reversed pattern of activation, with ventral posterior areas being activated first and then dorsal posterior areas, or activation of only ventral posterior areas that hold representations of the non-spatial feature [19]. In LaBerge’s model of attention, for example, when the location of the stimulus is predictable, parietal areas involved
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in coding spatial information can modulate featural information of an object in the occipito-temporal lobe by constricting the effective receptive fields of cells within this area, thereby aiding in the selection of the object with the attended feature [32,33]. In addition, the present study examined the relation between perceptual biasing and attentional modulation effects for spatial and non-spatial attention separately by comparing the neural source configurations underlying these effects. Based upon results of event-related fMRI studies, which have shown increased baseline activity in the same visual areas that were modulated by spatial attention (e.g., Refs. [22,26]), we expected to obtain similar source solutions for pre-target perceptual biasing and post-target attentional modulation effects. Lastly, the present study investigated the direction of attention in a condition where attention was to be directed simultaneously both to a location in space and to a color. If the two types of attention rely on completely different control structures, no interaction, but pure additive effects of directing attention to location and directing attention to color are expected. If, on the other hand, the two types of attentional control rely on similar mechanisms, simultaneously directing attention to location and color should place greater demands on these general control mechanisms as reflected by enhanced or prolonged attention directingrelated ERP effects. Another possibility would be that directing attention to a conjunction of location and color calls upon entirely new processes specific to the conjoining of the two stimulus attributes [54].
2. Method 2.1. Subjects Sixteen healthy volunteers participated in the study. Two subjects were discarded from the analyses because of poor eye fixation in the interval between cue and test stimulus or excessive blink activity during EEG recordings. Thus, 14 subjects (7 men, mean age of 23.2 years) remained in the sample. All subjects were students at the University of Amsterdam, were right-handed, had no history of mental or sustained physical illness, and had normal or corrected-tonormal vision by self-report. Subjects received credits as part of an introductory course requirement at the University of Amsterdam.
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a test stimulus (38 in height, 38 in width). This test stimulus was a blue or yellow square and appeared 7.138 to center from fixation in either the left or the right visual field and 1.738 to center above the horizontal meridian. The interval between test stimulus offset and onset of the next trial was varied randomly between 1400 and 2100 ms (rectangular distribution). During this interval, the fixation cross remained on the screen. All stimuli were presented on a black background. Within a run, subjects were randomly cued to attend to (a) a color (blue or yellow; color condition (COL)), (b) a location (left or right; location condition (LOC)), (c) a color and a location (e.g., blue and left; conjunction condition (CONJ)) or (d) to dnothingT (no-feature condition (N); see below). Each cue consisted of four white uppercase letters (all equal in width (0.368) and height (0.518)) presented around the fixation cross in a vertical array: dBT, dGT, dLT and dRT (see Fig. 1). Each letter corresponded to a stimulus feature: dBT to blue, dGT to yellow (dgeelT in Dutch), dLT to left and dRT to right. Letter order was counterbalanced across subjects with the restriction that the two blocationQ letters (dLT and dRT) and the two bcolorQ letters (dBT and dGT) were always grouped together, resulting in eight possible combinations of letters: BGLR, BGRL, GBLR, GBRL, LRBG, RLBG, LRGB and RLGB. In the color and location conditions, the color or location to which attention was to be directed, was indicated by two short, horizontal lines (0.208 in width, 0.088 in height), one on each side of a given letter (e.g., when presented next to dLT, attention had to be directed to the left (see Fig. 1)). In the conjunction condition, two letters, one representing a color, the other a location, were flanked by horizontal lines (0.108 in width, 0.088 in height) indicating that those both had to be used to direct attention. In the no-feature condition, the two horizontal lines (0.208 in width, 0.088 in height) were presented next to the fixation cross. Conjunction cues were presented on 40%, and color, location and no-feature cues each on 20% of the trials. In each task condition, the cue was followed by a test stimulus, which was presented for either 50 ms (standard duration; 75% of all trials in the attention-directing conditions, 87.5% in the no-feature condition) or 150 ms
2.2. Stimuli and procedure Each trial began with a 100-ms presentation of a cue (0.928 in width and 2.88 in height) that was located at fixation. After a random interval between 800 and 1500 ms (rectangular distribution), during which only the fixation cross (0.318 in width and 0.208 in height) was shown at the center of the screen, the cue was followed by
Fig. 1. Examples of cues used in the location (most left panel), color (second panel), conjunction (third panel) and no-feature (most right panel) conditions. Horizontal lines denote the letter-symbol(s) to be used to direct attention (L=attend left, R=attend right, G=attend to yellow, B=attend to blue). When presented next to the fixation cross (i.e., no-feature cue), no specific color or location had to be attended.
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(deviant duration; 25% of all trials in the attention-directing conditions, 12.5% in the no-feature condition). In case of an attention-directing cue, subjects were instructed to respond as fast and accurately as possible to test stimuli with the attended feature(s) that were presented slightly longer (i.e., 150 ms). On 50% of all trials, the test stimulus possessed the attended attribute. On 12.5% of all trials, therefore, target test stimuli were presented (with the attended attribute(s) and of longer duration). In case of a no-feature cue, subjects were asked to respond as fast and accurately as possible to test stimuli that were presented slightly longer (i.e., 150 ms), regardless of their color or location. Subjects used their right index finger to respond to targets. The experiment consisted of two sessions: a practice session and an EEG session. The aim of the practice session was to make subjects familiar with the specific task requirements and to make sure that they did not show excessive eye blink activity. It consisted of 8 runs of 80 trials (approximately 3.5 min each). During the EEG recording session, subjects sat in a comfortable chair with a computer monitor placed 80 cm in front of their eyes and positioned so that the vertical and horizontal straight-ahead lines of sight were the same for all subjects. After the electrode cap was placed, subjects practiced the task once and subsequently performed 24 task runs of 80 trials each while their EEG was recorded. Subjects were asked to minimize eye and body movements and allowed to pause between the runs if they wished to do so. 2.3. ERP recordings Recordings were made with 60 Ag-AgCl-electrodes mounted in an elastic cap: FP1, FP2, AF7, AF8, AF3, AF4, F7, F8, F5, F6, F3, F4, F1, F2, Fz, FT7, FT8, FC5, FC6, FC3, FC4, FC1, FC2, FCz, T7, T8, C5, C6, C3, C4, C1, C2, Cz, TP7, TP8, CP5, CP6, CP3, CP4, CP1, CP2, CPz, P7, P8, P5, P6, P3, P4, P1, P2, Pz, PO7, PO8, PO5, PO6, PO3, PO4, Poz, O1, O2, Oz and M1. All scalp channels were referenced to the right mastoid. Horizontal eye movements were monitored with two bipolar silver chloride electrodes placed on the left and right of the external canthi. Vertical eye movements and blinks were measured bipolarly with two silver chloride electrodes placed above and below the left eye. The EEG from each electrode site was DC recorded with a low-pass filter of 60 Hz and digitized (16 bits) at 250 Hz. Impedances were kept below 5 kV. The raw data files were filtered off-line with a 40-Hz low-pass filter (24 dB/oct, zero phase shift). Epochs were created starting 100 ms before and ending 800 ms after each cue of interest, and re-referenced to the mean of both mastoids. Epochs were automatically eliminated if the voltage exceeded F60 AV at the VEOG channel, F30 AV at the HEOG channel, or F60 AV at any of the other scalp electrodes. Four types of cue-locked ERPs were constructed next: COL (average across B and Y cues), LOC
(average across L and R cues), CONJ (average across BL, BR, YL and YR cues) and N (N cues). The EEG obtained in response to test stimuli was averaged for standard (i.e., test stimuli of short duration) trails only in the color and location single feature conditions. Four types of test stimulus-locked ERPs were constructed: color attended, color unattended, location attended and location unattended. Trials with incorrect responses (i.e., button press to non-target test stimulus) were not considered for averaging. The resulting average VEOG and HEOG cue-and test stimulus-locked waveforms were inspected for systematic deviations of eye position. If residual horizontal (N2 AV) or vertical eye movement-related activity (greater voltage at VEOG than FP1 or FP2) was present in the individual average ERP waveforms, the epoched segments were visually inspected and manually eliminated when contaminated with EOG activity. Two subjects, who showed systematic EOG activity on too many trials (i.e., N33% of the cue-locked epochs), had to be excluded from the analysis. 2.4. Behavioral analyses Repeated measures ANOVAs with the within-subject factor condition (COL, LOC, CONJ, N) were performed on response latencies of accurate responses to attended test stimuli of longer duration and arc sin-transformed omitted response rates. Furthermore, repeated measures ANOVAs with the within-subject factor attention-cue-condition (COL, LOC, CONJ) were performed on arc sin-transformed false alarm rates to (a) attended test stimuli, which were presented briefly, (b) unattended test stimuli, which were presented slightly longer, and (c) unattended test stimuli, which were presented briefly. These analyses were performed to test for differences in behavioral performance between cue conditions. 2.5. ERP analyses 2.5.1. Test stimulus-locked ERP analyses The ERPs elicited by attended versus unattended stimuli in spatial (P1 effect) and non-spatial (frontal selection positivity (FP), occipital selection negativity (ON)) attention tasks appear to be robust phenomena. Their presence was examined in the present report to confirm that subjects had indeed directed their attention to the cued stimulus feature(s). The P1-effect was investigated at electrodes P7 and P8 between 80 and 140 ms post-stimulus for the location condition. Voltage values, sampled every 4 ms within these intervals, were submitted to repeated measures ANOVAs, which tested for the effects of attention (attended, unattended; LOCATT), hemisphere (left, right; HEMI) and stimulus feature (left, right; LOC). The presence of FP and ON effects was examined, respectively, at electrodes F3 and F4 between 100 and 248 ms post-stimulus, and at electrode Oz, between 148 and 300 ms for the color condition.
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Voltage values, sampled every 4 ms within these intervals, were submitted to repeated measures ANOVAs, which tested for the effects of attention (attended, unattended; COLATT) and stimulus feature (blue, yellow; COL). In the FP analyses, the additional factor hemisphere (left, right; HEMI) was tested. Because of multiple interrelated comparisons, and hence the likelihood of false-positive spurious significant effects, for all analyses performed, effects were only considered reliable if they persisted for at least eight successive time bins (4 ms each, p-valueb0.05). 2.5.2. Cue-locked ERP analyses The 800-ms cue-target interval was divided into 40 time bins of 20 ms (5 sample points) and, for each time bin, the average voltage was computed for each electrode and task condition of interest. The average voltage values thus calculated were used as dependent variables in repeated measurements ANOVA analyses that were performed to isolate attentional control and/or domain-specific processes. First, in order to detect attention-related differences between the different cue conditions (COL, LOC, CONJ, N), mean voltage values were subjected as dependent variables to separate regional repeated measures ANOVAs (anterior analysis (F7/F8, F3/F4, FC5/FC6), central analysis (T7/T8, C3/C4, CP5/CP6) and posterior analysis (P7/P8, P3/P4, PO5/PO6)) for each time bin in the cue-target interval (0–800 ms post-cue). In these analyses, three factors were tested within subjects: cue condition (COL, LOC, CONJ, N; COND), electrode position within hemisphere (e.g., P7/8, P3/4, PO5/6; SITE) and hemisphere (left, right; HEMI). A main effect of condition or interaction effect of condition with any of the other factors would be indicative of a difference in attention-related processes between cue conditions. In case of a significant effect, post-hoc contrasts were used to determine which cue conditions specifically differed from one another. The following three orthogonal contrasts were specified for the factor COND: no-feature versus all three attention-directing cue conditions (attentiondirecting-related effect), conjunction versus single feature (i.e., average of color and location) cue conditions (interaction between spatial and non-spatial attentional control) and color versus location cue condition (attention domain-specific effect). Given our relatively small sample size, only results from dmixed-modelT tests were examined for all the repeated measurements analyses performed. The Huynh-Feldt or Greenhouse-Geisser epsilon correction factor (whenever the Huynh-Feldt epsilon was smaller than 0.75) was applied where appropriate, to compensate for possible effects of non-sphericity in the measurements compared. Only the corrected F- and probability values and the uncorrected degrees of freedom are reported. Because of multiple interrelated comparisons, and hence the likelihood of false-positive spurious significant effects, effects were only considered reliable if they persisted for at least two successive time bins (20 ms each, (corrected) p-valueb0.05).
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2.6. Source localization To investigate the spatio-temporal dynamics and the existence of domain specificity in attentional control, a subtraction logic and source modeling were applied (cf. Ref. [27]). For each electrode, six cue-locked grand average difference waves were calculated: (1) location-no-feature cue condition (single feature location (SFLOC)), (2) colorno-feature cue condition (single feature color (SFCOL)), (3) conjunction-color cue condition (conjunction location (CJLOC)), (4) conjunction-location cue condition (conjunction color (CJCOL)), (5) left-no-feature cues (single feature left (SFLEFT)) and (6) right-no-feature cues (single feature right (SFRIGHT)). The latter two contrasts allowed for the investigation of lateralization in the strength of effects with respect to the cued location. In addition, stimulus-locked attentional difference waveforms were created to investigate the relationship between attention directing-related effects and modulatory effect of attention on stimulus processing for the contrasts attended-unattended location stimuli and attended-unattended color stimuli. The following steps were then performed for each computed grand average difference waveform. The signal at each channel was first rereferenced to the average signal across all channels. Then, for each sample point, the global field power (GFP) was calculated as the square root of the sum of squares of the average-referenced activity over all channels. Peaks in the global field power function are indicative of high variance between channels and reflect a maximum of the total underlying brain activity that contributes to the surface potential field [36]. As a final step, one (or two, when the residual variance (RV) was still higher than 5%) bilateral dipole pair(s) with mirror-symmetric locations across hemispheres was fitted at GFP peak latencies (plus and minus two samples points (20 ms time bins)) of interest. Source models were determined using the BESA program (V.4.2). The default four shell ellipsoidal (i.e., head, scalp, bone, csf) was used. Each dipole was characterized by six parameters (three for location, three for orientation). The symmetry constraint with respect to location reduced the number of parameters to be fitted. An additional benergyQ constraint (weighted 20% in the compound cost function, as opposed to 80% for the RV criterion; see Ref. [2]) was used to reduce the probability of interacting dipoles (i.e., nearby dipoles producing high-amplitude potential fields of opposite direction). This criterion was maintained so as to favor solutions with relatively low dipole moments. Any difference in location and/or orientation parameters of the fitted dipole pair(s) between the color-no-feature and location-nofeature contrasts can be taken as evidence for a difference in neural mechanisms between the two types of attention. To evaluate apparent similarities/differences in equivalent dipole locations across the different conditions (e.g., SFLOC and SFCOL) at grand average GFP peak latencies, individual source parameters (dipole location, orientation and strength) were estimated and entered into ANOVA’s or
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paired t-tests. For a more detailed description of this procedure, see Kenemans et al. [27].
than in the COL (0.9%) and LOC (1.8%) conditions [ F(2,26)=6.154, p=0.006]. 3.2. ERPs
3. Results 3.1. Behavioral results There were no significant differences between the different task conditions in response latency (COL: 579, LOC: 576, CONJ: 567, N: 576 ms, relative to target onset) or the number of omitted responses to target stimuli (COL: 12.1%, LOC: 14.0%, CONJ: 13.8%, N: 15.5%). Neither were any difference observed between the different cue conditions in the number of false alarms to attended (COL: 1.4%, LOC: 1.7%, CONJ: 2.9%, N: 1.5%) or unattended (COL: 0.1%, LOC: 0.1%, CONJ: 0.1%) test stimuli of short duration. However, subjects made more false alarms to unattended test stimuli of long duration in the CONJ condition (4.2%)
3.2.1. ERPs to test stimuli As expected, P1 amplitudes were larger for stimuli presented at attended compared to unattended locations in the location condition between 112 and 140 ms poststimulus [6.2bF(1,12)b29.9, pb0.05] (see Fig. 2A). This difference in attention-related activity was larger over contralateral scalp regions as indicated by an interaction between attention (attended, unattended), hemisphere (left, right) and test stimulus feature (left, right) between 104 and 120 ms post-stimulus at electrodes P7 and P8 [5.6bF(1,12)b6.8, pb0.05]. Furthermore, compared to stimuli of the unattended color, stimuli of the attended color elicited a larger positive response at electrodes F3 and F4 between 128 and 228 ms in the color condition
Fig. 2. (A) Grand average ERP waveforms to attended (Att) and unattended (Unatt) test stimuli presented left or right from fixation for electrodes P7 and P8. (B, C) Grand average, average reference spline interpolated isopotential maps. Not shaded: areas of positive amplitude. Shaded: areas of negative amplitude. B: attended-unattended left test stimuli (left panel) and attended-unattended right test stimuli (right panel) at 120 ms post-test stimulus. (C) Left—no-feature cues (left panel) and right—no-feature cues (right panel) at 752 ms after cue onset.
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[5.7bF(1,12)b19.4, pb0.05] (see Fig. 3). In addition, a significant main effect of attention was observed at Oz between 152 and 188 ms [4.9bF(1,12)b39.7, pb0.05] reflecting a larger positive response to stimuli of the attended versus the unattended color. This positive response was followed by greater attention-related negativity, which, however, never reached significance. 3.2.2. ERPs to cues Fig. 4 shows the representative waveforms elicited by each type of cue (COL, LOC, CONJ, N) and the grand average difference waveforms for the color, location and conjunction effects (i.e., SFLOC, SFCOL, CJLOC and CJCOL). Potential distributions corresponding to the attention-directing-related effects are shown in Fig. 5. Table 1 lists time intervals and F-value ranges for main effects of COND and interactions between this factor and the factors HEMI and/or SITE within 0–800 ms post-cue, for each regional analysis. Each of the regional effects will be discussed next. The posterior analyses (electrode sites: P7/P8, P3/P4, PO5/PO6) revealed the earliest significant effect of condition. This effect was observed between 181 and 220 ms post-cue at
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posterior sites. Post-hoc comparisons and inspection of the data revealed that within this interval location cues elicited less negativity than color, conjunction or neutral cues (main effect of COND [2.9bF(3,39)b4.5, pb0.05]). This effect was followed by a more pronounced effect of condition between 261 and 500 ms post-cue at posterior sites (main effect of COND [4.6bF(3,39)b61.7, pb0.05]), which extended to more central scalp locations [321–400 ms: 5.8bF(3,39)b7.9, pb0.05]. Post-hoc comparisons and inspection of the grand average ERP waveforms showed that, in this interval, single feature cues elicited greater biphasic positivity than both nofeature and conjunction cues and, furthermore, that nofeature cues elicited greater positivity than conjunction cues at posterior sites especially during the early part of this biphasic positivity (261–400 ms post-cue). Scalp topographies of this early effect of cue condition show that it was maximal over lateral parietal and occipital sites (COND*SITE interaction [3.1bF(6,78)b7.8, pb0.05]) and that, during the first phase, the effect was more prominent at right compared to left posterior scalp locations, whereas during the second phase, it was more pronounced at left compared to right posterior scalp locations (COND*HEMI interaction [3.8bF(3,39)b6.9, pb0.05]). In the later part of the cue-target interval, starting at 661 ms, a third main effect of condition was observed for posterior scalp sites [3.4bF(3,39)b12.4, pb0.05]. This effect lasted until the end of the cue-target interval and reflected larger positive voltage over dorsal posterior sites for conjunction compared to single feature cues and greater positivity to single feature cues than nofeature cues over parieto-occipital sites (COND*SITE interaction [3.1bF(6,78)b7.8, pb0.05]). This late posterior effect spread to central scalp locations. A further effect of condition was observed over frontocentral scalp locations. Greater positive response was revealed to no-feature cues compared to attention-directing cues over central and anterior sites between, respectively, 401 and 640 ms [3.6bF(3,39)b15.7, pb0.05] and 441 and 600 ms [4.1bF(3,39)b17.3, pb0.05] after cue onset. This effect reflects a more anterior distribution of the posterior positivity in the no-feature compared to the other conditions. Lastly, the anterior analyses revealed a further difference between cue conditions: greater negativity to color cues compared to location, conjunction and no-feature cues [4.7bF(3,39)b10.5, pb0.05]. Between 641 and 760 ms, color cues elicited a larger negative response than location cues at frontal scalp locations. This effect was maximal over midline frontal electrodes. 3.3. Source localization
Fig. 3. Grand average ERP difference waveforms (attended–unattended color test stimuli) displaying the frontal selection positivity (FP) effect at electrode Fz. The grand average, spline-interpolated isopotential map (twodimensional projection) shows the topographical distribution of this effect at 144 ms post-test stimulus. The spacing between isopotentials in this map is 0.2 AV. White areas denote areas of positive amplitude and dotted areas denote areas of negative amplitude.
A close correspondence in GFP peaks and the abovedescribed statistically significant ERP effects was observed. At 184 ms post-cue, a small peak in GFP was only observed for SFLOC, followed by a bigger peak at 340 ms post-cue. The neural generators of these two effects (at 184 and 340 ms post-cue) were estimated first for the grand average
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Fig. 4. Top part: Grand average, cue-locked ERP waveforms for the different cue conditions for a selected number of electrodes. Bottom part: Grand average ERP difference waveform for the contrasts: conjunction–location cues (Conj-Loc; CJCOL), color–no-feature cues (Col-NF; SFCOL), conjunction–color cues (Conj-Col; CJLOC) and location–no-feature cues (Loc-NF; SFLOC).
difference waveform (SFLOC), and then for the individual subject difference waveforms, where the grand average solution parameters were used as a starting point (cf. Ref. [27]). Fitting of one symmetric dipole pair localized both effects to the ventral-lateral compartment of posterior cortex
[RV=4.0% (184 ms) and 1.6% (340 ms)]. No differences in location or orientation parameters were observed between the source models obtained at 184 and 340 ms for SFLOC. The main results of the grand average and per-subject estimation procedures for the 340 ms SFLOC effect are
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Fig. 5. Grand average spline-interpolated isopotential maps (two-dimensional projections) for the different contrasts at 180, 340, 520, 700 and 800 ms post-cue. Col=color cues, NF=no-feature cues, Loc=location cues and Conj=conjunction cues. The spacing between isopotentials is 0.3 AV. White: areas of positive amplitude. Shaded: areas of negative amplitude.
summarized in Fig. 6A and B (second panel). Furthermore, for both time points, no interaction was observed between the attention-direction of the location cue (SFLEFT, SFRIGHT) and hemisphere when dipole moments were compared, suggesting that the two effects were not lateralized with respect to the cued location. Inspection of the grand average GFP functions revealed that the second peak observed for SFLOC at 340 ms after cue presentation was also present for the other contrasts (SFCOL: 344 ms, CJLOC: 336 ms and CJCOL: 336 ms). One bilateral dipole pair with mirror-symmetric locations across hemispheres resulted in a model distribution explaining more than 95% of the variance in each of the recorded potential distributions [RV(SFCOL)=2.46%, RV(CJLOC)= 1.01% and RV(CJCOL)=0.70%]. The grand average and individual subject instantaneous source models for the different contrasts, which were derived at the d340T ms GFP peak latencies, are summarized in Fig. 6. Statistical analyses revealed that these dipoles did not differ significantly with respect to location across conditions.
This indicates that SFLOC, SFCOL, CJLOC and CJCOL have equivalent dipole locations in the lateral ventral posterior compartment of the cortex at around 340 ms postcue. The orientation of the dipoles, however, differed across conditions [in the left hemisphere: x: F(3,39)=7.1, y: F(3,39)=159.8, z: F(3,39)=20.0; in the right hemisphere: x: F(3,39)=9.8, y: F(3,39)=72.0, z: F(3,39)=8.1]. The dipole orientations for CJLOC and CJCOL were reversed (flipped around the x-, y- and z-axes) relative to the SFLOC and SFCOL dipole orientations. This effect reflects the fact that color and location cues elicited greater positivity over posterior scalp regions compared to both no-feature and conjunction cues. The exact reversal in orientation between the SFLOC and SFCOL, on the one hand, and CJLOC and CJCOL, on the other hand, illustrates the sensitivity of the modeling approach used in the present study (cf. Ref. [27]). For SFLOC and SFCOL, another GFP peak was observed at 532 and 544 ms, respectively. In this time window, a difference in positivity was observed over frontal
Table 1 Results from repeated measurement analyses at posterior, central and frontal electrode locations Posterior COND
COND*HEMI COND*SITE COND*HEMI *SITE
Central
181–220 261–500 661–800 241–380 281–780
2.9bF(3,39)b4.5 4.6bF(3,39)b61.7 3.4bF(3,39)b12.4 3.8bF(3,39)b6.9 3.1bF(6,78)b7.8
261–320 381–520 561–800
3bF(6,78)b4.1 2.7bF(6,78)b4.6 2.6bF(6,78)b4.5
Anterior
321–800
3.6bF(3,39)b15.7
421–800
2.9bF(3,39)b17.3
481–580 261–800
3.8bF(3,39)b8.1 2.8bF(6,78)b20.6
501–580 281–640 661–800
3.1bF(3,39)b7 2.8bF(6,78)b7.1 2.6bF(6,78)b5.1
Time windows are given for each significant effect ( pb0.05 for two successive time bins (i.e., 40 ms)) of condition (COND; SFLOC, SFCOL, CONJ, N), or of condition with hemisphere (HEMI; left, right) and/or electrode site (SITE), along with the minimum and maximum F-values for each effect.
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Fig. 6. (A) Grand average source solutions at d340T ms post-cue for the contrasts: location–no-feature cues (Loc-NF; SFLOC), color–no-feature cues (Col-NF; SFCOL), conjunction–color cues (Conj-Col; CJLOC) and conjunction–location cues (Conj-Loc; CJCOL). (B) Grand average (dark grey) and individual (black) dipole solutions at GFP peak latency d340T ms displayed for each contrast (i.e., Loc-NF, Col-NF, Conj-Col and Conj-Loc) separately.
and central scalp locations between single feature and nofeature cues. One bilateral dipole pair with mirror symmetric locations in posterior cortex gave a good fit for both contrasts [RV(SFLOC)=2.4% and RV(SFCOL)=1.4%] (see Fig. 7). Furthermore, their estimated source parameters did
Fig. 7. Grand average source solutions for color–no-feature cues (Col-NF; SFCOL) and location–no-feature cues (Loc-NF; SFLOC) for the early posterior (344 and 340 ms, respectively) and intermediate (544 and 532 ms, respectively) effects.
not differ, indicating that, at around 540 ms post-cue, similar areas of cortex were differentially activated by the two single feature cues versus the no-feature cue. These sources were located more medially ( p=0.015) and anteriorly ( p=0.004), and somewhat more dorsally than the sources that were estimated for the early posterior effects at around 340 ms post-cue.
Fig. 8. Grand average source solutions for color–no-feature cues (Col-NF (SFCOL); black dipoles) and location–no-feature cues (Loc-NF (SFLOC); dark grey dipoles) at 740 and 752 ms post-cue, respectively.
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Source modeling of SFLOC and SFCOL at GFP peaks at 752 and 740 ms post-cue, respectively, with one dipole pair with symmetric location parameters, localized both of these late effects of attentional control to the ventral posterior part of cortex [RV(SFLOC)=12.4%, RV(SFCOL)=5.0%]. As the RV for SFLOC in particular was relatively high, a second dipole pair was added to the source models. For both SFLOC and SFCOL, this second dipole pair moved to dorsal anterior cortex, whereas the ventral posterior dipole pair did not, or only slightly, change position (see Fig. 8). This time good fits were obtained for both SFLOC (4.5%) and SFCOL (2.3%). No differences in location parameters between SFLOC and SFCOL were found for the anterior or posterior sources. However, small differences in orientation of the dipoles were observed [anterior sources: z-orientation (left hemisphere): p=0.01, y-orientation (right hemisphere): p=0.01, posterior sources: z-orientation (left hemisphere): p=0.01], indicating that slightly different or more extended patches of anterior and posterior cortex may have been activated by location versus color cues in this latency range. Interestingly, comparison of dipole moments revealed a significant interaction between the attention-direction of the location cue (SFLEFT, SFRIGHT) and hemisphere at 752 ms postcue onset [ F(1,13)=5.4, p=0.018]. This effect reflects the fact that at this latency, right cues elicited significantly greater positivity in left compared to right ventral posterior cortex ( p=0.004), whereas left cues activated both ventral posterior regions to a similar extent (see Fig. 2C for the modeled scalp topographies). Fig. 8 summarizes the results from the grand average estimation procedures. 3.3.1. Relationship between late-latency cue effects and attentional modulation effects The ventral posterior sources of the 752-ms SFLOC and 740-ms SFCOL source models seemed very similar to sources estimated previously for, respectively, the P1 attentional modulation effect [3,14,42] and the color attentional modulation effects [1,35]. Also, the scalp topographies of the late posterior spatial attention-directing effect and the P1 selection effect were very comparable (see Fig. 2B and C). It was therefore examined whether the same ventral posterior areas that showed enhanced activation to attention-directing cues at the end of the cue-target interval were also modulated by attention. At 120 ms post, the difference in ERP between test stimuli presented at attended and unattended locations (i.e., the P1 selection effect) was best explained with a symmetric dipole pair in ventral-lateral occipital cortex and a single dipole in medial anterior cortex (RV=2.6%). Modeling of the P1 selection effect with just one symmetric dipole pair resulted in an implausible solution.1 The grand average 1 This is conceivably related to the fact that the attentional selection difference waveform was relatively noisy, as the individual difference waveforms consisted of an average of 58 trials only. The third dipole was added to model this noise.
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Fig. 9. Grand average ventral posterior sources of the late-latency attentiondirecting effects (left panel) and the first attentional modulation effects (right panel) for both spatial (A) and non-spatial (B) attention. Abbreviations: Col-NF=color–no-feature cues, Loc-NF=location–no-feature cues, Att=attended and Unatt=unattended.
ventral posterior source parameters of this and the late (752 ms) spatial attention-directing effect were very comparable (see Fig. 9A). However, paired t-tests on the individual subject source parameters indicated that the ventral posterior sources were located slightly more anteriorly for the P1 effect than the late-latency effect related to spatial attentional control ( p=0.025). At 144 ms, the difference in frontal positivity between test stimuli of the attended versus unattended color was best modeled with a symmetric dipole pair in the ventral central part of the brain (RV=6.7%) (see Fig. 9B). This dipole pair was located more anteriorly ( p=0.001) than the ventral posterior dipole pair estimated for the late-latency (i.e., 740 ms) effect of directing attention to color. The first effects of spatial (i.e., P1 effect) and non-spatial (i.e., FP effect) attention were thus located more anteriorly than the latelatency effects of directing attention to, respectively, location and color.
4. Discussion In this study, we investigated the nature and temporal dynamics of top-down attentional control. The extent to which the processes that direct the focus of attention depend on the to-be-attended stimulus dimension was assessed by comparing ERPs elicited by location and color attentiondirecting cues to ERPs elicited by no-feature reference cues. The neural source configurations underlying the thus observed spatial and non-spatial attention directing effects
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were investigated and directly compared to reveal possible differences in the configuration and/or timing of activated brain areas between spatial and non-spatial attentional control. Moreover, dipole modeling was used to explore the relation between perceptual biasing and attentional modulation effects. In addition, we examined attentional control in a condition where attention was to be directed to a conjunction of a color and a location. 4.1. The generality of attentional control Overall, very similar activation patterns were observed when attention was directed to location and color. The finding of closely corresponding ERP patterns to color and location cues is in line with results from recent event-related fMRI studies [13,50], which observed great overlap in the fronto-parietal networks involved in spatial and non-spatial attentional control within the same subjects. The present data supplement this functional anatomical knowledge by showing that the temporal sequence of activation within brain regions involved in attentional control is very similar for spatial and non-spatial attention. Multiple processes were linked to directing attention to location or color. Each of these effects is described below with regard to current neurophysiological models of attention. 4.1.1. Shortest-latency (184 and 340 ms) effects related to attentional control The shortest-latency differences in ERP between the single feature (color and location) conditions and the nofeature condition originated from ventral-lateral occipital cortex (see Fig. 6). These effects, greater positivity over parieto-occipital scalp regions, were already observed at 180 ms after the cue onset for the location condition, and at 260 ms for the color condition, and were largest at 340 ms for both conditions (see Figs. 4 and 5). Previous studies of spatial topdown control also found increased activation over posterior scalp regions in conditions where attention was directed to the left or right compared to a reference condition between 200 [15] or 250 [40] and 500 ms after cue presentation. The present findings show that this early posterior effect is generated in occipital areas, is not specific for the directing of attention to a location in space, but has a longer latency when attention is directed to color. They also are in line with results from a recent combined ERP and fMRI study, which located the earliest observed effect of directing attention to color (at 240 ms post-cue) to ventral-posterior cortex [28]. It could be argued on the basis of its source location in ventral-lateral occipital cortex that the enhanced posterior positivity reflects the biasing of the areas in which perceptual processing is modulated, rather than an attentional control process. However, this is contradicted by the fact that the early occipital activity was not lateralized with respect to the cued location. Results from single cell recording [38] and neuroimaging [22,26,60] studies generally support the notion that, just like the effects of spatial attention on target
processing [25,52,59], the increase in baseline activity is retinotopically organized. Therefore, the occipital effect at 340 ms after the cue onset likely does not reflect enhanced activity of feature-specific visual areas. Another, more probable, explanation for the differences in posterior positivity between single feature and no-feature cues is that it represents a dmeta-attentionT effect rather than enhanced preparatory activity of feature-specific visual areas. On both no-feature and attention-directing trials, upon sensory processing of the cue-symbol, the cue-symbol had to be mapped onto its corresponding task instruction. Yet, only in case of an attention-directing cue, this task instruction contained reference to a specific to-be-attended feature. So, only on attention directing trials, the link between the sensory information provided by the cue and its functional properties (i.e., the specific to-be-attended feature) had to be reinforced [12,23]. The enhanced activation of ventral posterior areas to single feature versus no-features cues may hence reflect increased activation of visual association areas that hold representations of the cuesymbol related to the invigoration of its functional significance in the single feature tasks. This explanation is in accordance both with the observed domain-independency of this early effect and the fact that it was not lateralized with respect to the cued location. It should be noted that this early effect does not simply reflect cue-symbol interpretation processes [60], as the no-feature cue had to be semantically interpreted as well. Attention thus seems to be set up by generic processes that are additional to cuesymbol interpretation processes and likely link the attentiondirecting cue to its associated test stimulus feature. 4.1.2. Intermediate-latency (540 ms) effects Between 400 and 640 ms post-cue, a difference in frontocentral positivity was observed between the single feature and no-feature cue conditions (see Fig. 5, third panel, first two rows). In this interval, attention-directing cues elicited greater negativity than no-feature cues. Mangun [40] also reported greater negativity to spatial attention-directing cues compared to neutral cues at central scalp sites between 500 and 700 ms after the cue onset. Here, this intermediate effect of directing attention was located to similar parts of posterior cortex for the location versus no-feature and color versus nofeature cue contrasts, indicating that directing attention to location and color relative to no specific feature resulted in increased activity in the same areas at this latency (see Fig. 7). It can accordingly be concluded that, at around 540 ms postcue, the same domain-independent processes were active in the color and location attention-directing cue conditions. The posterior sources estimated for the intermediate effects were located more anteriorly and medially than the sources found for the early posterior effects at 340 ms postcue (see Fig. 7). This may possibly reflect additional contributions from parietal or frontal areas to these effects. Recent event-related fMRI studies (e.g., Refs. [6,22,25]) revealed attention-directing cue-related activity in superior
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frontal cortex and superior and inferior parietal cortex. The present data suggests that these areas may be active relatively late after cue presentation, after processes related to sensory identification of the cue-symbol and linkage of the cue-symbol to the corresponding to-be-attended stimulus feature have completed. This would be in line with the common interpretation of these frontal and parietal activations as representing the actual execution of the task instruction, i.e. the directing of attention (e.g., Ref. [4]). 4.1.3. Late (~750 ms) posterior and anterior effects of directing attention to color or location and their relationship to the early attentional modulation effects FP and P1, respectively Dipole-source modeling revealed that slightly different or more extended patches of the same parts of dorsal anterior and ventral posterior cortex were activated by spatial and non-spatial top-down control at the end of the cue-target interval, as the location of the estimated anterior and posterior dipole pairs did not differ between the location and color attention-directing contrasts, but their orientations did (see Fig. 8). Hence, generic processes indifferent as to what feature was task-relevant were followed in time by processes that were in fact specific to the type of to-beattended feature. The difference in posterior dipole solutions may represent differences between spatial and non-spatial attentional control with respect to the precise neural populations showing pre-target preparatory activity, as, in case of spatial attention, dipole strength of the posterior dipole pair was lateralized with respect to the cued location, especially when attention was directed to the right hemifield. The close correspondence in scalp topography and laterality between this late posterior spatial attentiondirecting-related effect and the P1 selection effect and the similarity in their estimated source parameters provides further support for an interpretation of the late posterior effect in terms of preparatory activity of visual areas involved in the processing of the attended feature (see Figs. 2B,C and 9A). In line with this, previous studies using the high spatial resolution of fMRI have shown preparatory activity in the same visual areas that were modulated by attention (e.g., Refs. [22,26]). Yet, it is puzzling in this respect that the posterior sources estimated for the P1 spatial attentional modulation effect were located more anteriorly than those estimated for the late-latency effect of directing attention to location (see Fig. 9A). The same pattern of results was observed for nonspatial attention; the posterior sources estimated for the FP effect were located more anteriorly than those estimated for the posterior non-spatial attention-directing effect at the end of the cue-target interval (see Fig. 9B). One explanation for these unanticipated findings may be that lowering the threshold to task-relevant input in one brain area results in modulation of activity in the next area. It is noteworthy in this respect that while preparatory activity has been observed in V1 (e.g., Ref. [24]), this area is not modulated
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by selective attention (e.g., Refs. [3,43]). Albeit speculative, a similar mechanism might be at work for higher-level visual areas (i.e., preparatory activity leads to modulation at the next processing level) and explain the more anterior location of the posterior dipole pair for the test stimuluslocked attentional difference waveforms. The late-latency anterior dipoles were located close to premotor areas (see Fig. 8). Differences in their orientation between the location and color attention-directing contrasts likely reflects the domain-dependent effect observed between 640 and 760 ms after the cue onset at frontal electrodes. Next to the difference in early posterior positivity between the location and color cue conditions around 184 ms post-cue, this was the only other difference in cue-related ERP between the two types of top-down control. In this late latency time window, color cues elicited greater frontal negativity than location cues. Several fMRI studies have observed domain-dependent segregation of frontal cortex during the delay period (e.g., Refs. [13,51]). The difference in anterior dipole orientations between spatial and non-spatial attentional control is consistent with these findings and may hence reflect differences in maintenance processes between the spatial and non-spatial attention-directing cue conditions. To summarize, the present data indicate that the temporal sequence of activation within brain regions involved in directing the attentional focus is very similar for spatial and non-spatial attention.2 No evidence was found for differences in the timing of activation of dorsal and ventral posterior areas between spatial and non-spatial attentiondirecting cues as may be predicted based upon positionspecial theories [31,33,34,53,55,56]. The postulated special role of spatial attention in visual processing may arise from post-test stimulus differences between spatial and nonspatial attention in processes related to the detection of behaviorally relevant stimuli, rather than differences in goaldirected selection of stimuli. It may be argued that subjects were required to orient attention spatially in all conditions, even in the color cue condition, and that similarities in the location and color cue-related responses may therefore be due to the task design rather than to fundamental similarities in attentional control mechanisms. Yet, as we statistically compared ERPs elicited by color cues to ERPs elicited by no-feature cues, all putative activity related to dividing attention across the two peripheral locations where the test stimulus could be presented, should have been cancelled out. It is also important to note in this respect that results from a recent event-related fMRI study by Giesbrecht et al. [13] indicated that the brain regions involved in orienting 2 As one reviewer pointed out, it should be noted that since color and location cues were presented intermixed within the same run, attention had to be reset before the start of each trial at both the feature and dimension level. Differences in preparatory activity might have been more pronounced had the two types of cues been presented in separate runs and attention could have been tonically maintained at the dimension level.
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attention to color do not critically depend on whether the color stimulus is presented foveally or in the periphery. Brain activation patterns to color cues were virtually identical whether the task-relevant stimulus was presented at the fovea or in the periphery. This supports our reasoning that the observed overlap in location and color cue-related responses in the present study truly reflects similarities in attentional control mechanisms. All in all, the present findings suggest that, generally, the parts of the brain that extract the meaning of the cue and that are able to relate this to current goals generalize over the type of feature to-beattended. 4.2. Directing attention to a conjunction of color and location Attentional control was further investigated in a condition in which subjects were cued to direct attention to a conjunction of a location and a color. Conjunction cues initially elicited less posterior positivity than single feature location and color cues, but evoked greater central positivity from 540 ms on, as can be seen in Figs. 4 and 5. The delayed enhanced posterior positivity in the conjunction condition suggests that it may have taken longer to derive the information about the meaning of the cuesymbol in the conjunction compared to the single feature conditions. It is conceivable that it was more difficult to link the cue symbol to its associative properties (i.e., color and location) in the conjunction condition, as actually two symbols (letters) had to be used to direct attention in this condition. Starting at 540 ms and persisting throughout the rest of the cue-target interval, greater activation was observed over central scalp regions to conjunction compared to single feature cues (see Figs. 4 and 5, rows 3 and 4). No such central positivity was found for color versus no-feature cues or location versus no-feature cues. This topographical difference shows that directing attention to a conjunction of location and color is not simply the summation of directing attention to location plus directing attention to color, but may call upon extra brain mechanisms. These may be specific to the conjoining of two features, such as processes related to the integration of the spatial and non-spatial feature information [54] or processes representing the selective recruitment of frontal areas that simultaneously maintain spatial and object information on line [45]. Alternatively, the late central positivity to conjunction relative to single feature cues may reflect ongoing activity of brain regions involved in the control operations by which the cue-symbol is translated into a selective pattern of activation, related to the fact that in the conjunction condition two symbols had to be used to direct attention. More false alarms to test stimuli of longer duration were observed in the conjunction than the single feature conditions, suggesting that attentional control processes may indeed have taken longer to complete when two stimulus attributes were task-relevant.
5. Conclusions Our results indicate that a feature non-specific process, originating from ventral posterior cortex and possibly related to reinforcement of the link between attention-directing cue and its associated to-be-attended feature, initiates attentional control. They, furthermore, showed that this process takes about 340 ms to reach full strength when attention is to be directed to one stimulus feature. The brain areas involved in this cue association process are conceivably linked to occipital areas involved in preparatory processes and higher order areas in fronto-parietal cortex involved in maintenance. Which areas these are specifically seems to partially depend on the nature of the to-be-attended feature (i.e., color, location). Our results, in addition, suggest that directing attention to a spatial and non-spatial stimulus feature simultaneously involves a process that can be dissociated from the process of directing attention to a single feature. This process may be specific to the conjoining of a spatial and nonspatial stimulus feature or reflect ongoing activity of brain areas involved in the translation of the cue-symbol into a pattern of selective activation. Future studies combining the high temporal resolution of ERPs and the high spatial resolution of fMRI should further explore the sequence of brain activity involved in top-down control of spatial and non-spatial attention using a within-subject design and appropriate reference task.
Acknowledgments We would like to thank Marcus Spaan for his technical assistance and Durk Talsma and Tineke Grent-’t Jong for reading earlier versions of this manuscript. This research was supported by Dutch NWO grant 42520206 to A.K. and J.L.K.
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