Spatial attention and conscious perception: Interactions and dissociations between and within endogenous and exogenous processes

Neuropsychologia 50 (2012) 621–629

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Spatial attention and conscious perception: Interactions and dissociations between and within endogenous and exogenous processes ˜ b , Paolo Bartolomeo a,c,d Ana B. Chica a,b,∗ , Fabiano Botta b , Juan Lupiánez a

INSERM-UPMC UMRS 975, Brain and Spine Institute, Groupe Hospitalier Pitié Salpêtrière, Paris, France Department of Experimental Psychology, University of Granada, Spain AP-HP, Fédération de Neurologie, Groupe Hospitalier Pitié-Salpêtrière, Paris, France d Department of Psychology, Catholic University, Milan, Italy b c

a r t i c l e

i n f o

Article history: Received 5 May 2011 Received in revised form 22 December 2011 Accepted 24 December 2011 Available online 14 January 2012 Keywords: Spatial attention Endogenous Exogenous Conscious perception Event-related potentials ERPs

a b s t r a c t A current controversy exists about the relationship between spatial attention and conscious perception. While some authors propose that these phenomena are intimately related (Bartolomeo, 2008; Chun & Marois, 2002; O’Regan & Noë, 2001; Posner, 1994), others report dissociations between them (Kentridge et al., 1999; Koch & Tsuchiya, 2007; Wyart & Tallon-Baudry, 2008). However, spatial attention is not a unitary mechanism, and it is possible that not all forms of attention dissociate from conscious perception. In the present study we used a paradigm in which endogenous and exogenous forms of attention are orthogonally manipulated in order to investigate their relation with conscious perception within the same design. By analyzing two different cue-related components, our results demonstrated that while endogenous attention was electrophysiologically dissociated from conscious perception, exogenous attention was not, consistent with the hypothesis that exogenous attention is an important antecedent of our conscious experience. Our results support previous claims of dissociations between some forms of spatial attention and conscious perception, but also highlight the importance of exogenous orienting on the selection of information for conscious access. © 2012 Elsevier Ltd. All rights reserved.

1. Introduction It is now well established that a great amount of information reaching our senses can be processed at several levels of depth, even if it cannot be consciously reported (see e.g., Kouider & Dehaene, 2007). A fundamental question in the study of conscious perception (CP) involves the neurocognitive mechanisms determining or modulating the selection for consciousness. Attention has often been considered as one of the important mechanisms gating access to CP (Bartolomeo, 2008; Chun & Marois, 2002; O’Regan & Noë, 2001; Posner, 1994). Both attention and consciousness are complex concepts in search of consensus for definition. In the present study, we will refer to consciousness as ‘access’ to conscious report of a stimulus (Dehaene, Changeux, Naccache, Sackur, & Sergent, 2006). Thus, we will not deal here with forms of visual experience not amenable to verbal report (Dalla Barba, 2002; Edelman & Tononi, 2000; Merleau-Ponty, 1942). Attentional processes are also subserved by a partially heterogeneous set of different neurocognitive

∗ Corresponding author at: Departamento de Psicología Experimental, Facultad de Psicología, Universidad de Granada, Campus de Cartuja S/N, CP 18071, Granada, Spain. E-mail address: [email protected] (A.B. Chica). 0028-3932/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2011.12.020

systems. We will refer to attention as a mechanism for the selection of information, in its different varieties of orienting, alerting and executive control (Posner, 1994). In the present experiments, only spatial orienting will be manipulated. Behavioral and neuropsychological evidence supports the relationship between attention and CP. Right brain-damaged patients with spatial neglect are impaired in orienting attention towards contralesional, left-sided objects, with consequent unawareness of these stimuli (Bartolomeo, 2007; for a review). The hypothesis of a systematic relationship between spatial attention and CP has however been challenged by recent studies demonstrating that not all forms of attention are necessary for CP (Koch & Tsuchiya, 2007; see also Koivisto, Kainulainen, & Revonsuo, 2009). By using magnetoencephalography, Wyart and Tallon-Baudry (2008) have recently shown that endogenous spatial attention, as oriented by central arrow cues, can be electrophysiologically dissociated from CP (see also Kentridge, Heywood, & Weiskrantz, 1999, 2004; Kentridge, Nijboer, & Heywood, 2008; for behavioral dissociations). Attended or not, consciously perceived stimuli modulated mid-frequency gamma-band activity over the contralateral visual cortex, whereas spatial attention modulated high-frequency gamma-band activity, independent of whether targets were consciously perceived or not. Nonetheless, the orienting system of the human brain is not unitary. Spatial attention can be oriented either endogenously

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(i.e., top-down) or exogenously (i.e., bottom-up). These attentional systems are implemented in partially different brain regions (Chica, Bartolomeo, & Valero-Cabré, 2011; Corbetta & Shulman, 2002), and produce differential effects on information processing ˜ (Funes, Lupiánez, & Milliken, 2007; Klein, 2004, 2009). Previous behavioral (Chica, Lasaponara, et al., 2011), electrophysiologi˜ Doricchi, & Bartolomeo, 2010), cal (Chica, Lasaponara, Lupiánez, and functional magnetic resonance imaging research (Chica, PazAlonso, Valero-Cabré, & Bartolomeo, submitted for publication) with near-threshold targets has demonstrated that when attention is exogenously triggered, it is an important modulator of CP. Recent behavioral results, on the other hand, have also supported the view that endogenous attention is less important to CP, although it can well modulate CP after attention has been exogenously captured at the stimulus location (Chica, Lasaponara, et al., 2011). However, no study has so far compared the electrophysiological correlates of endogenous and exogenous attention and their relation to CP within the same experimental design. In the present study, we used a paradigm in which both endogenous and exogenous attention were orthogonally manipulated (Berger, Henik, & Rafal, 2005; Hopfinger & West, 2006). Participants were first presented with an informative central cue, which oriented spatial attention endogenously to one of the possible target locations. A non-informative peripheral cue (which exogenously captures attention to its spatial location) was then presented, followed by a near-threshold target. Target contrast was adjusted so that participants perceived only a proportion of the targets presented in each condition. Mean target contrast to report ∼50% of targets for each validity condition (endogenously and exogenously attended vs. unattended targets) was measured. Based on our previous results (Chica, Lasaponara, et al., 2011), we expected to find larger effects on CP for exogenous than for endogenous attention. Electroencephalogram (EEG) was also recorded in a sample of participants. We analyzed event-related potentials (ERPs) elicited by the peripheral cues. The key question to be answered is: Does the processing of the endogenous and exogenous cues influence CP of the subsequent targets? Cue-induced capture of attention might not be an all or none process. In each trial, cues might capture attention to a greater or to a smaller degree, perhaps depending on the state of preparation of the brain (Chica et al., 2010, submitted for publication). If attentional capture produced by exogenous cues, but not attentional orienting resulting from endogenous cues, were an important determinant of CP (Chica, Lasaponara, et al., 2011; Chica et al., 2010), then electrophysiological interactions between attention-related components and CP-related components are expected for exogenous spatial orienting, but not for endogenous orienting. Such a finding would constitute the first evidence of neural dissociations and interactions between different forms of spatial attention and CP within the same experimental design. 2. Methods 2.1. Participants Thirty-four participants gave their signed informed consent to participate in the study. Seventeen participants (8 women; mean age of 24 years, SD = 3.66) from Paris, France, participated in a behavioral session and received a monetary compensation for their time and effort. Seventeen further participants from Granada, Spain (6 women; mean age of 23 years, SD = 2.62) participated in the EEG study in exchange of course credit. The study was reviewed by the ethical committee of the Department of Experimental Psychology, University of Granada, and the INSERM review board, and received the approval of an ethical committee (Ile de France 1, Paris, France). 2.2. Apparatus and stimuli E-prime software was used to control the presentation of stimuli, timing operations, and behavioral data collection (Schneider, Eschman, & Zuccolotto, 2002). Participants sat at approximately 57 cm from the screen. In the behavioral task,

stimuli were presented on the screen of an eye tracker (Tobii Technology AB, Danderyd, Sweden; 17” wide, 1024 × 768, 16 ms refresh rate; temporal and spatial resolution of 50 Hz and 0.25◦ , respectively), against a grey background (Fig. 1A). Three horizontally aligned black markers (6◦ width × 5.5◦ height) were displayed. The two lateral markers were centered 8.5◦ to the left and right of the fixation point. The fixation point was presented inside the central marker and consisted of a black plus sign (0.5◦ × 0.5◦ ). The central and the peripheral cue consisted of a circle subtending 0.5◦ in diameter. The peripheral cue was always black, while the central cue could be either blue or yellow. For the central cue, one of the colors indicated that targets would likely appear on one side, while the other color indicated the other side (the assignment of color meaning to the left and right side was counterbalanced between participants). We used color instead of arrows as cues to be sure that attention was oriented purely endogenously (Funes et al., 2007). The central cue was presented at fixation, while the peripheral cue was presented in the upper-external part of one of the boxes. Matlab scripts were used to create 100 Gabor stimuli (4 cycles/deg. spatial frequency, 3◦ in diameter, SD of 0.3◦ ), with a maximum and minimum Michelson contrast of 0.92 (which we will refer to as 100% contrast, as it is the maximum contrast used in our manipulations) and 0.02 (1% contrast, minimum contrast used in our manipulations).

3. Procedure 3.1. Behavioral experiment Fig. 1A displays the sequence of a trial. In the behavioral experiment, the fixation display was presented for 2000 ms. The central cue was then displayed for 1200 ms. The central cue was spatially informative about the future location of the target in 67% of the target-present trials. Participants were informed about the predictive value of the central cue and were encouraged to take this information into account in order to respond more accurately. After disappearance of the central cue, the peripheral cue was randomly presented either at the left-sided location or at the right-sided one for 50 ms. Participants were informed that peripheral cues were useless to predict the side of the impending target and asked to ignore them. The inter-stimulus interval (ISI) between the peripheral cue and the target was 200 ms. The target was presented for 32 ms either at the left or at the right location, but never at the central location. Participants were required to perform two consecutive responses to the target. First, they were asked to discriminate the orientation of the Gabor lines (objective task) by pressing the “1” key in the numeric keypad of the keyboard if the lines were oriented to the left, and the “2” key if they were oriented to the right. Participants responded with their right hand, and were encouraged to respond to every trial as fast and as accurately as possible. Even if participants reported not having seen the stimulus, they were invited to try to guess their response. Afterwards, participants had to report if they consciously detected the appearance of the Gabor. This time, we encouraged participants to take their time to respond correctly. We presented participants with two arrow-like stimuli, one below and the other one above the fixation point (> > or < <). The vertical arrangement of the arrow-like stimuli ensured that participants could not prepare a lateralized response in advanced, associated to the location of the Gabor. We provided participants with 3 keys (to be pressed by using the left hand): an upper key (“d”), a lower key (“c”), and the space bar. The upper key always corresponded to the arrow presented above the fixation point, while the lower key was associated with the arrow presented below the fixation point. Participants were required to report as accurately as possible whether they had seen the target or not. If they had not, they were required to press the space bar. If they did see the target, they were asked to indicate its location on the screen (left or right). This procedure allowed us to know whether a false alarm corresponded to the same location as the previous cue (valid) or to the opposite location (invalid). Participants received feedback if no response was detected in the objective task, or if an anticipatory response occurred.

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Fig. 1. (A) Sequence of events in a given trial. (B) Sketch of the electrodes distribution around the scalp as viewed from above (the top of the figure represents the frontal area). Additional sites according to the 10–20 international system are shown for further reference.

Target contrast was manipulated before the experimental trials in order to adjust the percentage of consciously perceived targets at ∼50% for each validity condition separately. During practice trials, participants performed the above-described task. All participants started with a high-contrast stimulus (20% target contrast), which was well above the threshold of CP. Every 24 trials, the mean percentage of seen targets per validity condition (endogenously valid/exogenously valid trials, endogenously valid/exogenously invalid trials, endogenously invalid/exogenously valid trials, endogenously invalid/exogenously invalid trials) was calculated. If it was equal or higher than 55%, Gabors at the immediately following lower contrast level were used during the next 24 trials. Conversely, if the percentage of seen targets per condition was equal or lower than 45%, Gabors at the immediately following higher contrast level were used during the next 24 trials. This titration procedure continued until participants felt comfortable with the task, and target contrast yielded ∼50% seen targets for each of the four experimental conditions. Accuracy of the objective response was also titrated so that correct discrimination performance was between 65% and 85% (Gabor grating tilt orientation ranging between 1◦ and 10◦ ). To ensure that factors such as practice or fatigue did not influence CP, the same titration procedure operated every 32 trials during the whole experiment. Mean target contrast to report ∼50% of targets for each validity condition (endogenously and exogenously attended vs. unattended targets) was measured as the dependent variable of the subjective task. Participants were allowed to take a short break every 32 trials. During this break, they received feedback about the percentage of false alarms in the subjective task and their percentage of localization errors in the subjective task when it was larger than 33%. The experiment consisted of a total

of 560 trials. No target was presented on 20% of those trials. Therefore, there were 150 endogenously valid/exogenously valid trials, 150 endogenously valid/exogenously invalid trials, 74 endogenously invalid/exogenously valid trials, 74 endogenously invalid/exogenously invalid trials, and 112 catch trials. 3.2. EEG experiment In the EEG experiment, everything was the same as in the above-described behavioral experiment, with the following exceptions: Stimuli were presented on a 15-inch color VGA monitor; however, stimulus size was identical to the behavioral experiment. The fixation display varied randomly between 2000 and 2500 ms. The central cue was presented for a random duration of 1200–1500 ms. The peripheral-cue-to-target ISI also varied randomly between 200 and 300 ms.1 We included some trials in which only the peripheral cue was presented, and no response was required.2 Participants received feedback on the following conditions: If no response was detected in the objective task, if an anticipatory response was detected, or if they responded to those trials in which the central cue was not presented. Every 64 trials there was a pause, in which participants received feedback if either their percentage of false alarms or localization errors in the subjective task was larger than 33%. The experiment consisted of a total of 640 trials. No target was presented on 20% of

1 In previous research (Chica, Lasaponara, et al., 2011; Chica et al., 2010), a jitter had been added between the onset of the peripheral cue and target, without any measurable effects on the behavioral results produced by the peripheral cue. 2 These trials were added for the analysis of the central cue period, which is not reported in the present study.

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the experimental trials. On a further 20% of the trials, only the peripheral cue (i.e., neither the central cue nor the target) was presented. Therefore, there were 160 endogenously valid/exogenously valid trials, 160 endogenously valid/exogenously invalid trials, 80 endogenously invalid/exogenously valid trials, 80 endogenously invalid/exogenously invalid trials, 80 trials with no central cue, and 80 catch trials. The titration procedure was identical to the one used in the behavioral experiment. EEG was recorded using a 128-channel Geodesic Sensor Net of 129 Ag/AgCl electrodes (Tucker, Liotti, Potts, Russell, & Posner, 1994; see Fig. 1B). The head-coverage included sensors lateral to and below both eyes, to monitor horizontal and vertical eye movements. Impedances for each channel were measured and kept below 50 K before testing. All electrodes were referenced to the Cz electrode during the recording and were averaged rereferenced off-line. The EEG was amplified with a band pass of 0.1–100 Hz (elliptic filter) and digitized at a sampling rate of 250 Hz. EEG was filtered offline by using a 0.3–30 Hz band pass filter. Epochs were segmented from 200 ms before peripheral cue appearance to 250 ms after its presentation. All trials containing eye movements, blinks, or artifacts, as well as trials with anticipatory responses were rejected. A 200 ms segment prior to the cue presentation was used to calculate the baseline. Cue-related ERP analyses were performed over the following mean total of trials: Endogenously valid/exogenously valid seen (56) and unseen (51), endogenously valid/exogenously invalid seen (57) and unseen (50), endogenously invalid/exogenously valid seen (26) and unseen (28), endogenously invalid/exogenously invalid seen (25) and unseen (26). 4. Results and discussion In the behavioral experiment, participants broke fixation on 6% of the trials, which were eliminated from the analyses. In the EEG experiment, five participants were excluded from analysis because of a large number of false alarms (>54%), which made their subjective responses unreliable (2 participants), or because target contrast was not correctly adjusted at ∼50% for all conditions (3 participants). For the remaining participants, the rate of false alarms in the subjective task was 6% for the behavioral experiment, and 7% for the EEG experiment. 4.1. Behavioral results RTs faster than 150 ms in the objective task (0.60% and 0.16% of the trials for the behavioral and EEG experiment, respectively) were considered as anticipations and eliminated from the RT analysis. We performed an ANOVA on RTs for the objective task, with the factors of Experiment (Behavioral and EEG), Awareness (targets reported as “seen” or “unseen”), Endogenous Validity (valid vs. invalid) and Exogenous Validity (valid vs. invalid). The analysis demonstrated a main effect of Experiment, F(1,27) = 4.39, p = .046, with faster RTs for the behavioral than the EEG experiment. The interaction between Awareness and Experiment was also significant, F(1,27) = 4.31, p = .047, because RTs were faster for “seen” vs. “unseen” reports, but only in the behavioral experiment. More importantly, main effects of endogenous and exogenous attention were observed. RTs were faster at the endogenously attended vs. the endogenously unattended location, F(1,27) = 4.43, p = .045. Faster RTs were also observed for exogenously attended vs. unattended locations, F(1,27) = 8.48, p = .007 (see Table 1). None of the other main effects or interactions were significant. The analysis of the mean accuracy of the objective task only demonstrated a main effect of Awareness, F(1,27) = 456.91, p < .001. As expected, objective responses were at chance (M = .50) when participants reported not to have seen the targets, and well above chance (M = .74) when

targets were reported as being seen. None of the other main effects or interactions were significant. Mean target contrast (averaged contrast levels used during the experiment for each participant) was analyzed by using an ANOVA with the factors of Experiment (Behavioral and EEG), Awareness (“seen” vs. “unseen” reports), Endogenous Validity, and Exogenous Validity. Overall, target contrast was lower for the EEG than for the behavioral experiment, F(1,27) = 4.61, p = .041. These small differences in overall target perceptual contrast were expected, given the different experimental settings between the two experiments (e.g., the screens used and room luminosity). Target contrast was also lower for “unseen” than for “seen” targets, F(1,27) = 89.49, p < .001. Both main effects of endogenous and exogenous validity were significant (F(1,27) = 22.81, p < .001 and F(1,27) = 26.79, p < .001, respectively). Consistent with previous observations (see e.g., Liu, Abrams, & Carrasco, 2009; Pestilli & Carrasco, 2005), to consciously report ∼50% of the targets in each condition, target perceptual contrast proved significantly lower for valid than invalid trials, both when attention was endogenously, or exogenously oriented. The interaction between Awareness and Endogenous Validity was also significant, F(1,27) = 6.60, p = .016. Target contrast fulfilling the fixed threshold of 50% correct conscious detection (subjective task) proved to be lower for valid than for invalid trials, and this difference was larger for “seen” targets than for “unseen” ones. Although the percentage of seen targets was adjusted at ∼50% in each condition, there were small variations ranging between 53% and 61%. The above-described effects on target contrast perception might be influenced by these small differences in the percentage of seen targets per condition. For example, we observed that although target contrast was lower for endogenously valid vs. invalid locations, participants also reported fewer targets at the endogenously valid location (M = 55%) than at the invalid (M = 58%) location. To control for these trade-offs, we calculated an index by dividing target contrast by the percentage of seen targets per condition. This index therefore reflects genuine effects of attention on conscious perception of the target contrast. An ANOVA on these data with Experiment, Endogenous Validity and Exogenous Validity as factors demonstrated that the only significant effect was the main effect of Exogenous Validity, F(1,27) = 9.87, p = .004. The main effect of Endogenous Validity resulted far from significance, F < 1. This result indicates that exogenous attention is an important modulator of conscious perception of near-threshold targets, thus replicating previous results (Chica, Lasaponara, et al., 2011). 4.2. ERP results Event-related potentials (ERPs) locked to the appearance of the peripheral cue were analyzed. We split the trials in 4 conditions accordingly to the Endogenous and Exogenous Validity (endo valid/exo valid trials; endo valid/exo invalid trials; endo invalid/exo valid trials; endo invalid/exo invalid trials). These cue-related ERPs were calculated separately for trials that gave rise to “seen” or “unseen” reports. Visual inspection of cue-related ERPs revealed three main components during the cue period. The first component was the P100, peaking at 140 ms and observed in parieto-occipital electrodes, both ipsilaterally and contralaterally to the location of the cue. This component was followed by a frontal negativity (FNeg), peaking at 160 ms around the Fz electrode. Shortly afterwards, a negativity emerged (N100), peaking at 200 ms post peripheral cue onset in parieto-occipital electrodes, either ipsilaterally or contralaterally to the cue side. We calculated the mean amplitude of P100 (time window from 120 to 170 ms after the peripheral cue onset), FNeg (time window from 130 to 215 ms), and N100 (time window from 170 to 240 ms), for each participant in a sample of representative electrodes

Endo Invalid

0.16 0.15 0.14 0.16

Endo Valid Endo Invalid

7.90 8.64 7.49 8.04

Endo Valid Endo Invalid

8.59 9.40 7.99 8.56

Endo Valid Endo Invalid

0.52 0.51 0.51 0.50

Endo Valid Endo Invalid

0.74 0.76 0.78 0.77

Endo Valid Endo Invalid Endo Invalid

948 927

Endo Valid Endo Valid

904 911

Unseen Seen Unseen Seen

894 921

Unseen Seen

Target contrast ACC objective task RT objective task

EEG experiment

888 907 Exo Valid Exo Invalid

Seen

Target contrast/%Seen

0.17 0.18

Endo Invalid Endo Valid

0.16 0.18 9.21 9.82

Endo Invalid Endo Valid

8.75 9.41 9.85 10.29

Endo Invalid Endo Valid

9.18 9.74 0.49 0.50

Endo Invalid Endo Valid

0.50 0.51 0.73 0.71

Endo Invalid Endo Valid

0.73 0.72 766 785

Endo Invalid Endo Invalid

744 790

Endo Valid Endo Valid

835 891

Seen Seen

826 869 Exo Valid Exo Invalid

Seen

Target contrast/%Seen

Unseen Seen

Target contrast

Unseen ACC objective task

Unseen RT objective task

Behavioral experiment

Table 1 Mean RT (in ms) and accuracy (ACC) for the objective task, target contrast, and target contrast divided by the percentage of seen targets for each experimental condition of Awareness (“seen” and “unseen” targets), Endogenous Validity (endogenously valid and invalid trials) and Exogenous Validity (exogenously valid and invalid trials). Results for participants running the behavioral and EEG experiments are shown.

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covering the scalp (P3/P4, T5/T6, Pz/Cz, T3/T4, electrodes 12/5 representing Fz, F7/F8, Fp1/Fp2; see Fig. 1B). In order to determine the scalp location where each component was maximally elicited, we performed a one-way ANOVA for each component, with Electrode as a factor. For all three components, the main effect of Electrode was significant (all ps < .05). Consistent with previous results (see ˜ 2009; Hillyard, Luck, & Mangun, 1994), the e.g., Chica & Lupiánez, largest mean amplitude of the P100 component was observed in P3/P4 electrodes (M = 0.72 ␮), followed by T5/T6 electrodes (M = 0.47 ␮). These two amplitudes were statistically different (one-tailed t-test, p = 0.03). The largest mean amplitude of the FNeg component was observed in Fz electrodes (M = −0.37 ␮), followed by Pz/Cz electrodes (M = −0.29 ␮). These two amplitudes did not differ statistically (one-tailed t-test, p = 0.29). From all the sampled electrodes, Fp1/Fp2 were the only ones with negatives values in this time window. Fz electrodes, but not Pz/Cz, were significantly more negative than Fp1/Fp2 electrodes (p = 0.04 and p = 0.21, respectively). The largest mean amplitude of the N100 component was also observed in P3/P4 electrodes (M = −0.50 ␮), followed by Pz/Cz electrodes (M = −0.32 ␮). These two amplitudes were statistically different (one-tailed t-test, p = 0.05). We subsequently analyzed the modulation of each component for endogenous and exogenous attention when targets were or not consciously perceived by calculating its adaptive mean amplitude (20 ms before and after the higher peak) at those electrodes where the components were maximally elicited based on the previous analyses (P3/P4 electrodes for the P100 and N100 components, and Fz, Pz/Cz electrodes for the FNeg). For the P100 component, we performed an ANOVA including Awareness, Endogenous Validity, Exogenous Validity, and Electrode (ipsilateral vs. contralateral parieto-occipital electrodes, P3 and P4) as factors. This analysis demonstrated significant main effects of Awareness, Endogenous Validity, and a significant interaction between Awareness and Endogenous Validity (all ps < .05). All the previous effects were explained by the three-way interaction between Awareness, Endogenous Validity, and Electrode, F(1,11) = 6.11, p = .031. This interaction indicated that peripheral cues elicited a larger P100 component for subsequently “seen” vs. “unseen” targets, but only if the trial was endogenously invalid. This effect was larger for contralateral (Awareness × Endogenous Validity interaction, F(1,11) = 12.36, p = .005) than ipsilateral electrodes (Awareness × Endogenous Validity interaction, F < 1). We then analyzed the FNeg component observed in frontal electrodes. As it can be observed in Fig. 2A and B, FNeg was larger for “seen” than for “unseen” targets when the trial was exogenously valid (conditions 1 and 4 in Fig. 2A and B). In contrast, FNeg was larger for “unseen” vs. “seen” targets when the trial was exogenously invalid (conditions 2 and 3 in Fig. 2A and B). This was confirmed by an ANOVA with Awareness, Endogenous Validity, Exogenous Validity, and Electrode (Fz, Pz/Cz) as factors. The interaction between Awareness, Exogenous Validity and Electrode was significant, F(1,11) = 6.31, p = .029. Separate ANOVAs for Fz and Pz/Cz electrodes demonstrated that the Awareness × Exogenous Validity interaction was only significant for Fz electrodes, F(1,11) = 10.78, p = .007, whereas it was far from significance for Pz/Cz electrodes, F < 1. Tukey HSD post hoc comparisons for the interaction in Fz electrodes revealed that FNeg was significantly larger for subsequently “unseen” vs. “seen” targets when the trial was exogenously invalid, p = .025. Although the FNeg amplitude was larger for subsequently “seen” vs. “unseen” targets for exogenously valid cues, the comparison did not reached statistical significance, p = .624. The interaction between Awareness and Endogenous Validity was far from significance, F < 1. The FNeg component was therefore clearly related to exogenous orienting, and might indicate an efficient attentional capture by the peripheral cue.

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Fig. 2. Peripheral cue-locked analysis for each condition of Endogenous Validity, Exogenous Validity, and Awareness. (A) Topographic distribution of the FNeg effect, 160 ms after the peripheral cue onset. Results from left cues are presented for illustration. A schematic depiction of the relevant trial is also shown for each condition. Note that central cues consisted of color circles in the present experiments. Arrows are presented in the Figure for a simpler illustration. (B) Event-related cue-locked potential waveforms (time point 0 represents the moment of the peripheral cue onset), averaged for left- and right-presented cues, in Fz electrodes (12/5). (C) Topographic distribution of the cue-related N100 effect, 220 ms after the peripheral cue onset. Results from left targets are presented for illustration. A schematic depiction of the relevant trial is also shown for each condition. (D) Event-related cue-locked potential waveforms (time point 0 represents the moment of the peripheral cue onset) averaged for left- and right-presented cues, in electrodes P3/P4. Those electrodes which demonstrated an N100 effect are shown: ipsilateral electrodes for the Endo Valid/Exo Valid, Endo Invalid/Exo Invalid, Endo Valid/Exo Invalid conditions, and contralateral electrodes for the Endo Invalid/Exo Valid condition.

Finally, we analyzed the N100 component. As it can be observed in Fig. 2C and D, this parieto-occipital negativity was larger for “unseen” than for “seen” targets when the trial was endogenously valid (conditions 1 and 3 in Fig. 2C and D). In contrast, the parieto-occipital negativity was larger for “seen” vs. “unseen” targets when the trial was endogenously invalid (conditions 2 and 4 in Fig. 2C and D). An ANOVA (with Awareness, Endogenous Validity, Exogenous Validity, and Electrode as factors), revealed a reliable interaction between Awareness, Endogenous Validity, and Electrode, F(1,11) = 18.70, p = .001 (see below for more detailed analyses). The interaction between Awareness, Exogenous Validity, and Electrode was far from significance, F < 2.11. The parieto-occipital negativity was therefore clearly related to endogenous attention. We propose that this component indicates processing of the attended location (contralateral to the location of the component) just before the target was presented (Hillyard, Teder-Salejarvi, & Munte, 1998). That is, the presence of this component on the left hemisphere might indicate attentional orienting to the right hemi-space. First of all, it is important to note that when information provided by the central and peripheral cues was congruent (condition 1: endo valid/exo valid trials; and condition 2: endo invalid/exo invalid trials), the parieto-occipital negativity

was only observed when peripheral cues did not elicit the FNeg component (compare Fig. 2A–C). However, when information provided by the central and peripheral cues was incongruent (condition 3: endo valid/exo invalid trials; and condition 4: endo invalid/exo valid trials), the parieto-occipital negativity was only observed when the peripheral cues elicited the FNeg component. In conditions 1 and 2, information provided by central and peripheral cues was congruent. If we assume that peripheral cues properly captured attention when they elicited the FNeg component, we can propose that if peripheral cues captured attention, attentional orienting might be efficiently completed at an early time point, with no need for further additional processing. When, however, peripheral cues did not capture attention, the spatial information provided by endogenous and exogenous cues might not have been properly integrated. At the end of the orienting period, participants seemed to be paying attention to the location opposite to the direction indicated by the cues (e.g., in conditions 1 and 2 of Fig. 2C, participants appeared to allocate their attention to the right-sided, uncued location). This attentional orienting gave rise to “seen” reports if the targets were then presented at the attended (condition 2), but resulted in “unseen” reports if the targets were presented at the unattended location (condition 1).

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An ANOVA with the factors of Awareness, Validity, and Electrode (ipsilateral vs. contralateral electrodes) confirmed this result by showing a reliable interaction between Awareness and Validity, F(1,11) = 12.28, p = .005. Tukey HSD post hoc comparisons revealed a significantly more negative wave for subsequently “seen” targets than for “unseen” ones after invalid cues, p = .007. Although the effect was numerically reversed for valid cues, it did not reach significance, p = .879. When central and peripheral cues oriented attention to different locations (and therefore exogenous cues should be bypassed in order to effectively complete endogenous attentional orienting; conditions 3 and 4), this component was only elicited if peripheral cues captured attention (as again indicated by the FNeg component). Given that central and peripheral cues provided incongruent information, participants might have tried to re-orient attention to the location indicated by the central cue. In condition 3 (endo valid/exo invalid trials), participants were paying attention to the endogenously valid location at the end of the orienting period (i.e., the right-sided location in the example given in Fig. 2 for left-presented peripheral cues). However, when the target was presented at this attended location, it was not consciously perceived. In condition 4 (endo invalid/exo valid trials), participants were not able to re-orient attention to the location indicated by the central cue at the end of the orienting period, but they were able to perceive the target because it was presented at the location indicated by the peripheral cue. An ANOVA with the factors of Awareness, Validity and Electrode (ipsilateral vs. contralateral occipito-parietal electrodes) confirmed this hypothesis by showing a reliable interaction between the three factors, F(1,11) = 6.03, p = .032. The interaction revealed that N100 was more pronounced for subsequently “seen” vs. “unseen” targets at contralateral vs. ipsilateral electrodes in condition 4 (endo invalid/exo valid trials), F(1,11) = 5.35, p = .041. In condition 3 (endo valid/exo invalid trials), the interaction did not reach significance, F(1,11) = 2.08, p = .178. This result indicates that while endogenous attention was clearly dissociated from conscious reports of near-threshold targets, exogenous attention was instead related to target reportability.3 5. General discussion The aim of this study was to directly compare the effects of different forms of spatial orienting (endogenous vs. exogenous) on conscious reports. The experimental paradigm we used allowed us to manipulate both types of orienting within the same trial and to measure CP of near-threshold targets. Behaviorally, both endogenous and exogenous attention produced significant RT modulations on the objective task, demonstrating that our manipulation was effective in orienting attention in both modes. Importantly, however, only exogenous attention produced a reliable enhancement of conscious reports in the subjective task. This result replicates our previous observations indicating that

3 Target contrast values were lower for “seen” than for “unseen” targets, and also for validly cued than for invalidly cued targets (with both endogenous and exogenous cues). Importantly, however, our results cannot be explained by these small differences in target contrast. For example, the cue-related FNeg component was larger at the endogenously valid/exogenously valid location for “seen” targets (where target contrast was the lowest) and at the endogenously invalid/exogenously invalid location for “unseen” targets (where target contrast was the highest). This might invite the conclusion that the FNeg component was contaminated by target perceptual contrast, being larger for “seen”/high-contrast targets, and smaller for “unseen”/low-contrast targets. However, this conclusion is not supported by the results of the remaining two conditions. Even though for the endogenously valid/exogenously invalid and endogenously invalid/exogenously valid conditions, target contrast was identical, the FNeg component was larger for “seen” targets in the endogenously valid/exogenously invalid condition, but it was instead larger for “unseen” targets in the endogenously invalid/exogenously valid condition. The same line of reasoning applies for the cue-related N100.

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exogenous attention produce larger modulations on the conscious perception of near-threshold targets than endogenous attention does (Chica, Lasaponara, et al., 2011). In our previous ERP study (Chica et al., 2010), we observed that a cue-related P100 component was strictly linked to subsequent conscious reports. For valid trials, the cue-related P100 was larger for subsequent “seen” than for “unseen” reports; for invalid trials, the reverse was true. A similar ERP modulation was observed in the present study, but for an FNeg component peaking around 160 ms after the peripheral cue presentation. This difference in the ERP component related to CP is likely due to differences in experimental design. While in our previous research (Chica et al., 2010) only exogenous peripheral cues were presented, in the present design peripheral cues were preceded by central informative cues, which were likely to change the state of the system before peripheral cues were presented. In particular, in the present experiments, exogenous cues had to be integrated with previous endogenous cues. Endogenous orienting likely requires the activity of prefrontal structures (Alivisatos & Milner, 1989; Bartolomeo, Siéroff, Decaix, & Chokron, 2001; Buschman & Miller, 2007; Koski, Paus, & Petrides, 1998); the integration of prefrontal activity with more posterior activity generated by exogenous cues might account for the more anterior localization of the pattern we observed in the present study, as compared to our previous results obtained with exclusively exogenous cues. The FNeg component was clearly modulated by exogenous attention and correlated with subsequent conscious reports. This component seems to be related to the attentional capture produced by the peripheral cue, because it was larger for subsequently “seen” vs. “unseen” targets when peripheral cues were valid, while the effect reversed for invalid cues. This result clearly confirms that exogenous attention is an important modulator of CP, and that the state of the attentional system before the target is presented influences our conscious experience. Just before target appearance, we observed a parieto-occipital negativity that was likely related to endogenous orienting of attention to the contralateral side of space (Hillyard et al., 1998). When endogenous and exogenous cues were congruent (i.e., they were either both valid or both invalid), and this component indexed the orienting of attention to the invalid location, participants missed the targets with valid cues, but consciously reported them after invalid cues. This evidence further suggests a relationship between spatial attention and CP. However, given that both endogenous and exogenous attention were oriented to the same location, it is not possible to disentangle the respective contributions of each attentional system. Nevertheless, our design also included conditions in which endogenous and exogenous attention were oriented to different spatial locations, thus allowing us to disentangle the contribution of each type of orienting to CP. Under these incongruent cueing conditions, we observed that when endogenous cues were valid and exogenous cues invalid, orienting attention to the location indicated by the central cue led to “unseen” rather than “seen” reports. In the opposite situation, with invalid endogenous and valid exogenous cues, orienting attention to the location of the peripheral cue resulted in “seen” rather than “unseen” reports. This finding constitutes further and more direct evidence of the important role of exogenous attention, rather than endogenous orienting, for CP. There might be several mechanisms underlying the differential modulation exerted by exogenous and endogenous attention on CP. One possibility is that peripheral cues might initiate some activity at the corresponding spatial location (they might for example ˜ open an “object file”; Lupiánez, 2010; Milliken, Tipper, Houghton, ˜ & Lupiánez, 2000). Peripheral cues might also serve as “spatial anchors”, such that targets subsequently presented at that location have priority access to CP. Exogenous attention is most effective in enhancing CP when endogenous attention is subsequently oriented to the same location (Chica, Lasaponara, et al., 2011). The extent

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to which an “object file” representation is used for further performance might thus depend on its ability to predict target appearance at a similar location, a piece of information that might be integrated within the same representation. Endogenous attention might thus exert its modulatory role by stabilizing activity related to the perceptual object, for example by facilitating recurrent processing from frontal to parietal nodes of the attentional network (Lamme, 2006). Finally, exogenous attention is strictly related to alertness, with which it shares partially overlapping networks in the right hemisphere (Sturm & Willmes, 2001). Consistent with this notion, phasic auditory alerting induced by a short auditory stimulus has been shown to improve visual conscious perception in healthy participants (Kusnir, Chica, Mitsumasu, & Bartolomeo, 2011), as well as in brain-damaged patients with spatial neglect (Chica, Thiebaut de Schotten, et al., 2011; Robertson, Mattingley, Rorden, & Driver, 1998). Peripheral cues are automatically processed, even when they are not consciously reported (McCormick, 1997; Mele, Savazzi, Marzi, & Berlucchi, 2008), and their effects are short lasting (Müller & Rabbitt, 1989). This fast and mandatory processing could be at the basis of the interaction between phasic alerting and exogenous spatial orienting produced by the appearance of the cue. On the other hand, the occurrence of central-symbolic cues also produce phasic alerting, but cue interpretation takes a longer time. Therefore, once spatial attention is oriented to the cued location, alerting is still not maximal, and only the isolated effects of spatial orienting, rather than its interaction with phasic alerting, are observed. This might explain why, if central cues are easier to interpret (such as arrow cues, which are the object of extended practice in our cultural environment), behavioral modulations of CP can be observed, although there may still exist neural dissociations (Wyart & Tallon-Baudry, 2008). At the neural level, neuroimaging studies have encountered difficulties to dissociate the neural basis of endogenous and exogenous orienting. The insufficient temporal resolution of techniques such as functional magnetic resonance imaging prevents the capture of fast and brief cerebral events, such as exogenously driven attentional orienting. Studies on brain-damaged patients have revealed that after right hemisphere damage leading to left visuospatial neglect, there is a dramatic lack of consciousness of stimulation presented contralaterally to the brain lesion, which is associated to substantial deficits in exogenous orienting with relative sparing of endogenous orienting (Bartolomeo & Chokron, 2002). Importantly, neglect patients’ lesions typically involve the right parietal lobe (Mort et al., 2003) and its connections with prefrontal cortex (Bourgeois, Chica, Migliaccio, Thiebaut de Schotten, & Bartolomeo, in press; Bartolomeo, Thiebaut de Schotten, & Doricchi, 2007). Activity of such fronto-parietal networks has been shown to be implicated both in orienting attention (Buschman & Miller, 2007; Corbetta & Shulman, 2002; Nobre, 2001) and CP (Dehaene et al., 2006). Recent transcranial magnetic stimulation results have also causally implicated the activity of the right temporo-parietal junction (a component of a ventral fronto-parietal attentional network) in exogenous but not in endogenous orienting (Chica, Bartolomeo, et al., 2011). Taken together, these results suggest that activity within the ventral attentional network (which is typically impaired in neglect; Corbetta, Kincade, Lewis, Snyder, & Sapir, 2005) is associated to exogenous spatial attention and CP. Future research is needed in order to better understand the conditions under which spatial attention modulates conscious perception, as well as the temporal course and the brain mechanisms supporting their interactions. Acknowledgements Supported by postdoctoral grants from the Neuropôle de Recherche Francilen (NeRF), Marie Curie Intra-European Program

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