Isolating neural correlates of conscious perception from neural correlates of reporting one's perception — TEI-tagged view

PittspersName, MetzlerpersName, HillyardpersName (2014date). “Isolating neural correlates of conscious perception from neural correlates of reporting one's perception.” Frontiers in Psychologytitle·j.

Object of study — the neural correlate of conscious perceptionterm, and the fact that measuring it requires the subjectterm to reportterm·mth - which brings its own neural processes with it

Research question — which candidate NCCsterm survive when awarenessterm and task-relevanceterm are crossed, so that a stimulusterm can be consciously seen without being accessed for reportterm·mth

Contribution — the P3bterm and the late occipital positivity track accessterm for reportterm·mth rather than awarenessterm; only the early sensory components and the 200-240 ms negativity are present whenever the stimulusterm is seen and absent whenever it is not

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Isolating neural correlates of conscious perceptionterm from neural correlates of reporting one's perception Michael A PittspersName Michael A PittspersName 1 Department of Psychology, Reed College, Portland, OR, USA 1, * , Stephen MetzlerpersName Stephen MetzlerpersName 1 Department of Psychology, Reed College, Portland, OR, USA 1 , Steven A HillyardpersName Steven A HillyardpersName 2 Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA 1 Department of Psychology, Reed College, Portland, OR, USA 2 Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA Edited by: Talis Bachmann, University of Tartu, Estonia Reviewed by: Giorgio Marchetti, Mind, Consciousness, and Language Research Net, Italy; Jaan Aru, University of Tartu, Estonia ✉ *Correspondence: Michael A. PittspersName, Department of Psychology, Reed College, 3203 SE Woodstock Blvd Portland, OR 97202, USA e-mail: mpitts@reed.edu This article was submitted to Consciousness Research, a section of the journal Frontiers in Psychology.

Received 2014 Jun 14; Accepted 2014 Sep 8; Collection date 2014.

Copyright © 2014 PittspersName, MetzlerpersName and HillyardpersName.

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PMCID: PMC4189413 PMID: 25339922 Abstract To isolate neural correlates of conscious perceptionterm (NCCsterm), a standard approach has been to contrast neural activity elicited by identical stimuli of which subjectsterm are aware vs. unaware. Because conscious experience is private, determining whether a stimulusterm was consciously perceived requires subjective reportterm·mth: e.g., button-presses indicating detectionterm, visibility ratings, verbal reportsterm·mth, etc. This reporting requirement introduces a methodological confoundterm when attempting to isolate NCCsterm: The neural processes responsible for accessing and reporting one's percept are difficult to distinguish from those underlying the conscious percept itself. Here, we review recent attempts to circumvent this issue via a modified inattentional blindnessterm·mth paradigmterm·mth (PittspersName et al., 2012 ) and present new data from a backward maskingterm·mth experiment in which task-relevanceterm and visual awarenessterm were manipulated in a 2 × 2 crossed design. In agreement with our previous inattentional blindnessterm·mth results, stimuli that were consciously perceived yet not immediately accessed for reportterm·mth (aware, task-irrelevant condition) elicited a mid-latency posterior ERPterm negativity (~200–240 ms), while stimuli that were accessed for reportterm·mth (aware, task-relevant condition) elicited additional components including a robust P3bterm (~380–480 ms) subsequent to the mid-latency negativity. Overall, these results suggest that some of the NCCsterm identified in previous studies may be more closely linked with accessing and maintaining perceptual information for reporting purposes than with encoding the conscious percept itself. An open question is whether the remaining NCCterm candidate (the ERPterm negativity at 200–240 ms) reflects visual awarenessterm or object-basedterm attentionterm.

Keywords: attentionterm, awarenessterm, maskingterm·mth, task-relevanceterm, VANterm, P3bterm Introduction Determining the neural basis of consciousness is one of the most challenging problems in modern cognitive neuroscience. Much progress has been made over the past 25 years by simplifying the problem and focusing first on identifying neural correlates of conscious perceptionterm or “NCCsterm” (Baars, 1989 ; Logothetis and Schall, 1989 ; Crick and Koch, 1990 , 2003 ). The primary strategy has been to compare brain activity elicited by physically identical stimuli of which subjectsterm are aware vs. unaware. While appealing in its simplicity, this approach has recently been criticized for being too inclusive in what counts as an NCCterm (Aru et al., 2012 ; de Graaf et al., 2012 ). Depending on how awarenessterm is manipulated, neural mechanisms that are necessary-but-not-sufficient or sufficient-but-not-necessary for conscious perceptionterm have often been misinterpreted as true-NCCs. Aru et al. ( 2012 ) refer to such neural processes as “pre-requisites” and “consequences” of conscious perceptionterm, respectively, and have encouraged researchers to develop new paradigmsterm·mth to help distinguish the “NCC-proper” from these related, yet functionally distinct, processes.

Terminology and theoretical considerations While the central tenets of Aru et al.'s ( 2012 ) proposal are well-justified, we prefer to use the terms “pre-consciousterm” and “post-perceptualterm” instead of “pre-requisite” and “consequence.” In our view, the term pre-requisite is too general and the term consequence too restrictive. For example, retinal processing could be considered a pre-requisite of visual awarenessterm (with the exception of TMS-induced phosphenes); however, no one has proposed retinal activity as a potential NCCterm. The term pre-consciousterm , instead, is used here to refer only to cortical and cortico-thalamic activity following the initial feedforward activation of primary sensory cortex. Pre-consciousterm processing immediately precedes (both temporally and functionally) conscious processing and is capable of establishing elaborate perceptual representations that may become conscious (Dehaene and Naccache, 2001 ; Dehaene et al., 2006 ). The term consequence, on the other hand, appears to be used by Aru and colleagues to refer to certain neural events that necessarily follow the conscious awarenessterm of a stimulusterm. In contrast, the term post-perceptualterm leaves open the possibility that conscious perceptionterm may occur with or without these subsequent processing events. As outlined below, simple manipulations of the task can eliminate post-perceptualterm processing while leaving conscious perceptionterm intact.

It should also be noted that the term “perceptual awarenessterm·def” (often abbreviated as “awarenessterm”) will be used here to describe situations in which perceptual content is reportable, although actual reporting may not take place, e.g., because the subjectterm has been instructed to only reportterm·mth awarenessterm of certain types of stimuli. This reportability requirement is commonly used to operationally define conscious perceptionterm but differs from certain theoretical frameworks that consider some types of perceptual processing as “phenomenally conscious” even if the subjectterm is unable to reportterm·mth anything about these percepts when specifically instructed to do so (Lamme, 2006 ; Vandenbroucke et al., 2014 ). It also differs from notions of phenomenal consciousness in which perceptual content is accessible, yet not necessarily accessed (Block, 2007 , 2011 ). In both cases, we consider such processing as “pre-consciousterm” rather than a special type of unreportable consciousness, and our main goal is to isolate neural correlates of “accessterm consciousness” from correlates of pre-consciousterm and post-perceptualterm processing (Dehaene and Changeux, 2004 , 2011 ; Block, 2005 ; Dehaene et al., 2006 ). Because the term “accessterm” can have different meanings in different contexts, we will qualify its usage for clarity, e.g., “conscious accessterm” typically refers to global availability of perceptual information for flexible use by a variety of cognitive systems, while “access of perceptual information for reportterm·def” refers to a much narrower set of post-perceptualterm operations involved in task-related memory and decision-making processes.

While it is important to separate both pre-consciousterm and post-perceptualterm activity from correlates of conscious perceptionterm, the current study focuses mainly on post-perceptualterm processing. To illustrate the problem of conflating neural correlates of post-perceptualterm processing with correlates of conscious perceptionterm, it is useful to consider “the refrigerator door problemterm·def” (a neural counterpart to the “refrigerator light illusion” described by Block, 2001 ). Imagine you have no accessterm to the internal machinery of a refrigerator and your goal is to determine under what conditions the light inside the refrigerator turns on. You might start by opening the door to check and proceed to try just opening it a crack or just for a brief moment. However, every time you open the door the light is always on and you can't be sure the light would have been on if you had kept the door closed. In consciousness research, one of the goals is to determine whether unique brain signal X correlates with conscious perceptionterm (the light turning on), but to do so requires a perceptual reportterm·mth from the subjectterm (opening the door). The problem is that it is often difficult to determine whether the same brain signal X would have occurred if the subjectterm had not accessed this information for reportterm·mth (kept the door closed).

Post-perceptualterm processing in paradigmsterm·mth that manipulate visual awarenessterm To manipulate visual awarenessterm in the lab, the most commonly used paradigmsterm·mth include backward maskingterm·mth, the attentional blink, change blindness, binocular rivalry, and signal detectionterm at thresholdterm (e.g., Pins and ffytche, 2003 ; Fernandez-Duque et al., 2003 ; Sergent et al., 2005 ; Koivisto et al., 2006 ; PittspersName et al., 2010 ). In all cases, subjectsterm are asked to provide some type of perceptual reportterm·mth after each trial. These reportsterm·mth range from identification of target stimuli to detailed visibility ratings such as using a perceptual awarenessterm·def scale (Ramsøy and Overgaard, 2004 ). At first glance, this method of requiring a subjective reportterm·mth after each trial seems unproblematic. Regardless of whether the stimulusterm was consciously perceived, the subjectterm always has to reportterm·mth something even if the reportterm·mth is “I saw nothing.” Indeed, in many paradigmsterm·mth, stimuli are visible on roughly half of the trials, and there would be no means of sorting trials into aware vs. unaware conditions without trial-by-trial reportsterm·mth. However, upon closer scrutiny, aware vs. unaware contrasts in paradigmsterm·mth such as these are likely to expose not only differences in brain activity related to conscious perceptionterm but also differences in post-perceptualterm processing. On aware trials, subjective reportsterm·mth rely on the maintenance of perceptual information in working memoryterm and accessterm of this information by higher-level cognitive systems that enable decision-making and response planning/execution. On unaware trials, there is no conscious perceptual information to maintain or accessterm even though a decision must be made and a negative response must be planned and executed. Thus, in addition to differences in conscious perceptionterm, these two types of trials differ in terms of post-perceptualterm processing such as maintenance in working memoryterm and accessterm of perceptual information for decision-making.

Figure 1 provides a simplified schematic outline of some of the stages of processing likely to be involved in aware vs. unaware trials for a typical backward maskingterm·mth experiment in which the stimulusterm (e.g., an outline square) is perceived on roughly half of the trials. Note that in addition to differences in visual awarenessterm, the two trial types also differ in post-perceptualterm processing, thus any differences in neural activity between aware and unaware trials may reflect post-perceptualterm maintenance and accessterm for reportterm·mth instead of awarenessterm per se . Importantly, the attentional blink, change blindness, signal detectionterm, and a number of other paradigmsterm·mth are vulnerable to this same confoundterm.

Figure 1.

Simplified schematic depicting some of the stages of processing involved in the two main trial types of a typical backward maskingterm·mth experiment in which the stimulusterm is masked at a constant SOA (e.g., 50 ms) and is visible on roughly 50% of trials . In addition to differences in conscious perceptionterm, post-perceptualterm processing is likely to differ across the two trial types due to the task demands.

The sustained inattentional blindnessterm·mth paradigmterm·mth As an alternative to these more commonly employed paradigmsterm·mth to manipulate awarenessterm, we recently adapted the inattentional blindnessterm·mth paradigmterm·mth, originally developed and extensively tested in behavioral studies by Mack and Rock ( 1998 ), for use in conjunction with electrophysiological recordings of brain activity (PittspersName et al., 2012 ). This paradigmterm·mth includes three experimental phases. In the first phase, subjectsterm perform a distracter task while a critical (unexpected) stimulusterm is presented directly in the center of their view. After 200 or more presentations of the critical stimulusterm, the subjectsterm are queried regarding their awarenessterm of this stimulusterm. Typically, about half of all subjectsterm reportterm·mth a complete lack of awarenessterm of the critical stimulusterm and are thus deemed inattentionally blind in this first phase. Importantly, after being asked about the critical stimulusterm, subjectsterm are instructed to “continue performing the same task as before” in the second phase of the experiment. Due to the intervening questions, all subjectsterm become aware of the critical stimulusterm during phase 2, but because they are performing the same distracter task they do not need to accessterm information about the critical stimulusterm for immediate perceptual reportterm·mth. Finally, in the third phase of the experiment, subjectsterm are instructed to forego the distracter task and perform a discrimination task in which the critical stimulusterm becomes task-relevant.

This modified inattentional blindnessterm·mth paradigmterm·mth allows comparisons of brain activity across three conditions in which awarenessterm and post-perceptualterm processing are manipulated in a step-wise fashion: phase 1 = unaware; phase 2 = aware without post-perceptualterm processing (critical stimulusterm is task-irrelevant); phase 3 = aware with post-perceptualterm processing (critical stimulusterm is task-relevant). Figure 2 sketches a simplified overview of the stages of processing involved in the three phases of this inattentional blindnessterm·mth paradigmterm·mth.

Figure 2.

Outline of the modified inattentional blindnessterm·mth paradigmterm·mth used by PittspersName et al. ( 2012 ) . Because the critical stimulusterm (square shapeterm) is task-irrelevant in phases 1 & 2, post-perceptualterm processing is avoided while allowing a contrast that better isolates differences in conscious perceptionterm. Neural correlates of post-perceptualterm processing can be evaluated by comparing phases 3 & 2.

The contrasts of interest in this three-phase experiment are between brain activity elicited by the critical stimulusterm in phase 2 vs. phase 1 (i.e., awarenessterm vs. unawareness of task-irrelevant stimuli) and phase 3 vs. phase 2 (i.e., task-relevant vs. task-irrelevant stimuli). The first contrast (phase 2 vs. 1) should reveal neural correlates of conscious perceptionterm per se , while the second contrast (phase 3 vs. 2) isolates correlates of post-perceptualterm processing (maintenance in working memoryterm and accessterm for reportterm·mth). It should be noted that direct comparisons of brain activity across phases would be of questionable validity because the ordering of the three phases cannot be counterbalanced and neural activity may differ due to repeated exposure to the stimuli, neural fatigue, sensory adaptation, etc. To circumvent this issue, a control stimulusterm (e.g., a randomized background having no shapesterm or features) can be randomly intermixed with the critical stimuli in each phase, and neural responses to the critical stimulusterm can first be contrasted with neural responses to the control stimuli within each phase prior to making across-phase comparisons. Also, in order to prevent contamination by pre-motor and motor-related activity, the critical stimuli are never targets that require manual responses, even in the third phase of the experiment. Instead, an infrequent target stimulusterm is also intermixed in all phases of the experiment, and during the third phase subjectsterm must discriminate between the critical (non-target) stimulusterm and this target stimulusterm in order to respond appropriately.

Pre-consciousterm, conscious, and post-perceptualterm EEG signatures in the sustained inattentional blindnessterm·mth paradigmterm·mth Using this modified inattentional blindnessterm·mth paradigmterm·mth, a potential NCC-proper was isolated from pre-consciousterm and post-perceptualterm activity (PittspersName et al., 2012 , 2014 ; PittspersName and Martinez, 2014 ). Event-related potentials (ERPsterm) elicited by shapeterm stimuli (formed by oriented line elements) were compared to randomly oriented control stimuli across the three phases of the experiment. During all three phases (including inattentional blindnessterm·mth), an initial occipital negativity was evident from ~160–220 ms. We interpreted this activity as pre-consciousterm because it was evident even when subjectsterm did not reportterm·mth any conscious awarenessterm of the shapeterm stimuli due to inattentional blindnessterm·mth induced by performing the distracter task. We initially referred to this component as “Nd1” for “negative difference 1” (PittspersName et al., 2012 ), but have subsequently labeled it “CINterm” for “contour integration negativityterm·def” (PittspersName and Martinez, 2014 ), on the assumption that it reflects pre-consciousterm neural activity associated with extracting contour information from the stimulusterm array. In the second and third phases (aware conditions), the CINterm was followed by a bilateral occipital-parietal negativity from ~200–300 ms (initially labeled “Nd2”), which was similar in timing and scalp topography to the previously reported “visual awarenessterm negativity” or “VANterm” component (Koivisto and Revonsuo, 2010 ; Railo et al., 2011 ). Importantly, this negativity was also elicited during phase 1 in the group of subjectsterm who later reported having spontaneously noticed the (irrelevant) shapeterm stimulusterm. When the shapeterm stimuli were task-irrelevant, no ERPterm differences were evident subsequent to the VANterm, as subjectsterm were not required to further process this information. In the third phase, however, the VANterm was followed by a selection negativity (SNterm) and two late positive components (a late occipital positivity “LOP,” and the centro-parietal P3bterm) as well as by induced gamma oscillations (PittspersName et al., 2012 , 2014 ). We interpreted these latter effects as post-perceptualterm because they were absent in the second phase (aware, task-irrelevant) and present in the third phase (aware, task-relevant).

In a subsequent experiment (Shafto and PittspersName, 2013 ), we tested a different critical stimulusterm, line drawings of faces, in a similar inattentional blindnessterm·mth paradigmterm·mth. Here, we found that the face-specific N170 component as well as the VANterm were absent during inattentional blindnessterm·mth (phase 1) but were present in both aware conditions (phase 2 and 3). Consistent with the results from the shapeterm experiment, the SNterm, LOP, P3bterm, and induced gamma oscillations were only evident in the third phase in which the face stimuli were task-relevant. Importantly, in both experiments we were able to compare brain activity in aware vs. unaware conditions (phase 2 vs. phase 1-unaware subjectsterm) without requiring immediate accessterm for perceptual reportterm·mth. This was accomplished by presenting the stimuli well above thresholdterm (300 ms duration, easily visible if expected) and by delaying the perceptual reportterm·mth until after the entire block of trials (which lasted ~10 min and delivered 200+ stimuli). In both the shapeterm and face experiments, subjectsterm who were initially inattentionally blind often expressed genuine surprise at having failed to notice such salient stimuli for 10 min, and many subjectsterm reported “not being able to avoid noticing the stimuli” once they knew the stimuli were being presented (in phase 2). These design features are critical in paradigmsterm·mth in which trial-by-trial perceptual reporting is intentionally avoided; i.e., one must be certain that the critical stimuli are never seen during the unaware condition and that these same stimuli are obvious and readily visible during the aware condition, even when subjectsterm are performing a separate task.

This modified inattentional blindnessterm·mth paradigmterm·mth shows promise in helping to distinguish pre-consciousterm and post-perceptualterm activity from the NCC-proper. Future fMRI and intra-cranial EEG studies should consider adopting similar methods. However, one drawback with the inattention paradigmterm·mth is that it only includes 3 of the possible 4 combinations of visual awarenessterm and task-relevanceterm; i.e., the unaware, task-relevant condition, which is common in other awarenessterm paradigmsterm·mth, is absent in the inattentional blindnessterm·mth paradigmterm·mth. This missing condition, in which a stimulusterm is attended and relevant to the task but not consciously perceived, may be important for separating neural correlates of awarenessterm from neural correlates of attentionterm. It is also advantageous to cross-validate results by employing more than one type of experimental paradigmterm·mth, and the above mentioned results have only been obtained so far using the inattentional blindnessterm·mth approach. The current study was designed to address these outstanding issues.

A 2 × 2 manipulation of visual awarenessterm and task-relevanceterm in a maskingterm·mth paradigmterm·mth One option for measuring NCCsterm using the maskingterm·mth paradigmterm·mth is to present stimuli for a brief duration followed by a mask such that the stimulusterm is consciously perceived on approximately 50% of trials (Koivisto et al., 2008 ). This approach allows comparisons of brain activity on aware vs. unaware trials while the physical stimuli (stimulusterm + mask) remain identical. Of course, with this approach all stimuli must be task-relevant because the experimenter has no other means of sorting individual trials into aware and unaware conditions. A different approach is to employ two different maskingterm·mth latencies (i.e., stimulusterm durations), one that is very short leading to 0% awarenessterm and another that is considerably longer resulting in 100% awarenessterm (Koivisto and Revonsuo, 2008 ). In this variation of the maskingterm·mth paradigmterm·mth, task-relevanceterm can be manipulated, and trial-by-trial reporting is unnecessary. However, the use of two different mask-onset latencies introduces another problem, namely that brain activity is likely to differ due to physical stimulusterm differences as opposed to a difference in awarenessterm (Bachmann, 2009 ). For example, ERPsterm elicited by a mask presented 16 ms after a stimulusterm will be superimposed with ERPsterm elicited by the stimulusterm, whereas a mask presented 300 ms after a stimulusterm will only affect the stimulus-elicited ERPsterm at latencies beyond ~350 ms. To control for this confoundterm, a control stimulusterm can be presented and masked at each of the two latencies, and the ERPsterm elicited by the control stimuli can be subtracted from the ERPsterm elicited by the stimuli of interest prior to making any aware vs. unaware contrasts. The subtraction essentially removes the mask-elicited ERPterm that is superimposed with the stimulus-elicited ERPterm. This was the approach used in the current study, which compared stimuli of 16 ms (unaware) vs. 300 ms (aware) duration, each of which was either task-relevant or task-irrelevant on separate blocks of trials. The overall design was similar to a previous study that compared ERPsterm elicited by masked vs. unmasked letters while spatial and non-spatial attentionterm were manipulated (Koivisto and Revonsuo, 2007 ).

Here, the stimuli were contour shapesterm, colored lines, and control stimuli consisting of a random array of lines (Figure 3A ). We first performed a behavioral detectionterm study in which these stimuli were masked at 5 different latencies (i.e., stimulusterm durations of 16, 33, 50, 67, and 300 ms). Based on the results from this experiment, two maskingterm·mth latencies (16 and 300 ms) were selected for the EEG experiment because these mask-onsets showed close to 0 and 100% detectionterm rates, respectively, for both shapeterm and colorterm stimuli. In the EEG experiment, on separate blocks of trials, shapesterm or colored-lines were deemed task-relevant, and the shapeterm, colorterm, and control stimuli were masked at each of the two latencies. This design allowed comparisons of ERPterm difference waves (shapeterm minus control, colorterm minus control) across 4 types of trials: aware, task-relevant; aware, task-irrelevant; unaware, task-relevant; unaware, task-irrelevant.

Figure 3.

Stimuli and methods used in the current experiment . Five types of stimuli (A) were presented in the EEG experiment (C) while awarenessterm was manipulated via short vs. long masking SOAsterm·var (16 or 300 ms). Task-relevanceterm of the square and 4-red-line stimuli was manipulated by altering the target detectionterm task. An initial behavioral experiment (B) was conducted to evaluate stimulusterm visibility at five different masking SOAsterm·var.

Methods Participants Twenty-six healthy adults participated in the EEG experiment. All were recruited as volunteers and gave informed consent prior to the beginning of the experiment. Data from eight participants were later excluded; three due to excessive EEG artifact, and five due to awarenessterm of some of the 16 ms colorterm stimuli, as assessed by a behavioral post-test (see below). The final group consisted of 18 participants (mean age: 21 years old; 13 female). An initial behavioral experiment was conducted to determine the masking SOAsterm·var used in the EEG experiment. Twelve (different) subjectsterm participated in this behavioral study; data from one subjectterm was excluded from analyses due to failure to follow task instructions. All experimental procedures were approved by the Reed College institutional review board in compliance with the Declaration of Helsinki.

Stimuli and procedure Stimuli consisted of 20 × 20 arrays (visual angle = 6.2 × 6.2°) of oriented white line segments (0.34°), identical to those used in PittspersName et al. ( 2012 , 2014 ). In the inter-stimulus intervals (ISIs) the lines were visible and in randomized orientations. Upon each stimulusterm presentation all of the lines rotated to new positions for the specified duration. For control stimuli, the line elements shifted to new random orientations. Two types of shapeterm stimuli were created by arranging the new orientations of subsets of line segments to form a 10 × 10 square or a 7 × 7 diamond. Two types of colorterm stimuli were created by changing either 3 or 4 of the randomly oriented line segments from white to red (RGB: 255,0,0). The spatial locations of the red lines were randomized but constrained to overlap with the locations of the shapeterm contours to control for spatial attentionterm·var across the shapeterm and colorterm tasks (see procedure below). Across trials, the positions of the red lines varied but were restricted to occur in upper, lower, left, and right regions with no two red lines being located in the same region. Example stimuli are shown in Figure 3A . For both the behavioral experiment and the EEG experiment, the line element arrays were always visible; no blank inter-stimulus intervals (ISIs) were used. Each stimulusterm presentation was followed by a return to a new pattern of randomly oriented line segments, which served as the maskingterm·mth/ISI stimuli; each ISI lasted a random interval between 1000 and 1200 ms. A central fixation cross (0.5°) was present at all times. All stimuli were presented on a dark background (0.07 cd/m2) on an LCD monitor (refresh rate = 60 Hz). Stimuli were created and displayed using Presentation software (Neurobehavioral Systems, Albany, CA).

In the behavioral experiment (Figure 3B ), three different stimuli were presented: square shapesterm, 4-red-lines, and random (control) arrays. The diamond and 3-red-line stimuli were not presented because these stimuli would eventually serve as targets in the EEG experiment, while the ERPsterm of interest would be for the non-target stimuli (squares, 4-red-lines). Each stimulusterm was followed by a maskingterm·mth (ISI) stimulusterm at 5 equiprobable stimulusterm onset asynchronies (SOA): 16.67, 33.34, 50, 66.67, and 300 ms. Thus, there were 15 combinations of stimulus-type and mask SOA, and each combination was presented 20 times. The subjectterm's task was to press a response button with their right index finger whenever they perceived either colorterm or shapeterm. Subjectsterm were encouraged to adopt a liberal response criterion, responding even if they just caught a glimpse of colorterm or shapeterm, while avoiding guessing. The goal of this experiment was to determine a masking SOAterm·var that would render both colorterm and shapeterm invisible for all subjectsterm on all trials. It was also important to verify that the 300 ms stimuli could be detected on 100% of trials.

Based on the results from the behavioral experiment, two different masking SOAsterm·var were employed in the EEG experiment (16.67 and 300 ms), resulting in 10 different stimulus-mask combinations: (2 types of shapeterm stimuli + 2 types of colorterm stimuli + 1 random control stimulusterm) × (2 mask SOAs) = 10 combinations. During each block of trials, these 10 trial types were intermixed and presented in random order, each at 10% probability. On separate blocks of trials, subjectsterm performed either a colorterm or a shapeterm task. In the colorterm task, the target stimuli were 3-red-lines and in the shapeterm task, the diamond stimuli served as targets. Subjectsterm pressed a response button with their right index finger upon target detectionterm. In order to control for between-condition ERPterm differences associated with motor preparation and execution, all target trials (and any trials in which subjectsterm responded) were excluded from ERPterm analyses. Each task was performed for 900 trials (~15 min) before switching to the other task for 900 trials, and this sequence was then repeated (task-orderterm·var was counterbalanced across subjectsterm). For example, half of the subjectsterm performed the colorterm task for 15 min, switched to the shapeterm task for 15 min, switched back to the colorterm task for 15 min, and finished with 15 min of the shapeterm task. Thus, 1800 total trials were completed for each task, 180 of each stimulusterm type. Figure 3C shows a summary of the EEG experiment design, and a video example of the stimulusterm sequence is provided in Movie 1 .

Because the behavioral experiment revealed detectionterm rates greater than zero for the 16.67 ms colorterm stimuli in some subjectsterm, an additional behavioral post-test was conducted after each EEG session. In this post-test, colorterm stimuli (4-red-lines), shapeterm stimuli (squares), and control stimuli (random arrays) were presented and masked at 16.67 or 300 ms. A total of 180 stimuli were presented (across three 1 min blocks), 30 trials of each stimulus-mask combination. As in the behavioral study, subjectsterm were instructed to press a button whenever they detected either colorterm or shapeterm (employing a liberal response bias). Five of the 26 participants detected 16.67 ms colorterm stimuli on at least one trial during this post-test and were excluded from ERPterm analyses. No subjectsterm detected any of the 16.67 ms shapeterm stimuli, nor were there any “false alarm” responses to the randomized control stimuli. Active experiment time for the EEG study was ~60 min, short rest breaks were provided after every 60 trials (~1 min), and longer breaks were given after every 300 trials (~5 min). Each experimental session lasted 3.5–4.5 h including EEG cap preparation, practice trials, rest breaks, and the behavioral post-test.

EEG recording and ERPterm pre-processing EEG was noninvasively recorded from the scalp via Ag/AgCl electrodes sewn into customized caps with 96 electrode placements (EASYCAP, Herrsching, Germany). Electrode locations were modified from the standard 10–20 system to allow equidistant spacing (electrode positions reported here refer to the nearest channels of the international 10–20 system). Electrode impedances were kept below 5 kΩ. Signals were digitized (at 500 Hz) and amplified by three 32 channel amplifiers (Brain Amp Standard, Brain Products, Gilching, Germany). Eye movements and blinks were monitored by left and right horizontal EOG channels and a vertical EOG channel under the left eye, respectively. An electrode positioned at CPz served as the reference during recording.

ERPsterm were time-locked to the line segment orientation changes, low-pass filtered at 25 Hz (24dB/Oct), re-referenced to the average of the left and right mastoids, and baseline corrected from −100 to 0 ms. The left and right horizontal EOG channels were re-referenced as a bipolar pair. Trials were discarded if they contained eye movements, blinks, or other muscle artifacts in a −600 to +600 ms interval surrounding stimulus-onset. Artifact detectionterm was accomplished semi-automatically via per-subject adjustment of the following peak-to-peak thresholdsterm: eye movements (50 μV, 50 ms steps, in bipolar HEOG), blinks (100 μV, 200 ms steps, in VEOG and FP1), and muscle noise (150 μV, 200 ms steps, all remaining channels). On average, 16% of trials were rejected due to a combination of these artifacts. Individual electrodes showing extended periods of noise in the raw EEG were removed and replaced by interpolated signals from surrounding channels using topographic spherical splines (channels included in ANOVAsterm·stat were not interpolated).

ERPterm analyses Our strategy for ERPterm analyses was to first identify time windows and electrodes of interest in the grand-averaged difference waves of all conditions averaged together, using our previous results as a guide (PittspersName et al., 2012 ). Peak latencies were identified and mean amplitudesterm were assessed in ± 20 ms time windows around these peaks (± 50 ms for the broad P3bterm). The electrode showing the maximal signal, along with 5–8 adjacent sites (according to each component's scalp topography), were selected for analysis. For the shapeterm stimulusterm difference waves (shapeterm minus random), four distinct components were evident, each of which closely matched our previous results in terms of timing and scalp distribution: contour integration negativityterm·def, “CINterm” (160–200 ms), visual awarenessterm negativity, “VANterm” (200–240 ms), late occipital positivity, “LOP” (310–350 ms), and the “P3bterm” (380–480 ms). For the colorterm stimulusterm difference waves (colorterm minus random), four components were also evident, some of which showed reduced latencies compared to the corresponding shape-elicited components. The first color-elicited component showed a very similar time course and scalp topography to a previously reported colorterm vs. non-color ERPterm difference (Schoenfeld et al., 2003 ). This component, which consisted of a midline ventral-posterior negativity accompanied by a vertex positivity from 130 to 170 ms, has previously been referred to as the “sensory effect of colorterm·def” which we abbreviate here as “SEC” (Zinni et al., 2014 ). The SEC (130–170 ms) was followed by the VANterm (200–240 ms), LOP (290–330 ms), and P3bterm (380–480 ms) components, each of which showed similar scalp topographies to their shape-elicited counterparts.

Statistical analyses began with 2 × 2 ANOVAsterm·stat with the factors awarenessterm (16 or 300 ms durations) and task-relevanceterm (attended or unattended) for each difference wave component using the time windows specified above. Difference wave amplitudesterm were averaged across electrode clusters according to the scalp topographies of each component as follows: CINterm [ PO4, P6, O2, PO8, O10, PO10 ]; SEC [ FC1, FCZ, FC2, C1, CZ, C2, CPZ ]; VANterm [ PO4, P6, O2, PO8, O10, PO10 ]; LOP [ P1, PZ, P2, PO3, POZ, PO4, O1, OZ, O2 ]; P3bterm [ CP1, CPZ, CP2, P1, PZ, P2, POZ ].

All main effects and interactions were then further explored by conducting cluster mass permutation teststerm·stat on the difference amplitudesterm (shapeterm minus random; colorterm minus random) for each of the 4 conditions separately ( aware, task-relevant ; aware, task-irrelevant ; unaware, task-relevant ; unaware, task-irrelevant ). To increase statistical power, separate tests were carried out for the early (100–300 ms) and late (300–600 ms) time windows and permutation analyses were restricted to 63 of the 96 electrodes (covering central, parietal, temporal, and occipital regions) based on a priori hypotheses regarding scalp topographies of each component. Thus, 6363 comparisons were made for the early time window and 9450 for the late time window. In all cases, two-tailed cluster mass permutation teststerm·stat (Bullmore et al., 1999 ), with a family-wise alpha level of 0.05, were conducted using the original data and 2500 random within-subject permutations of the data. Electrodes within approximately 3.02 cm of one another were considered spatial neighbors. All cluster mass permutation analyses were carried out using the mass univariate ERPterm Toolbox (Groppe et al., 2011 ).

Results Behavioral experiment Mean shape and color detection ratesterm·var at each of the five masking SOAsterm·var tested are provided in Figure 4 . Overall, the shapeterm stimulusterm was more readily masked than the colorterm stimulusterm. Eight of the 11 subjectsterm never responded to shapesterm presented for 16 ms, two subjectsterm responded once (5%) and one subjectterm twice (10%); note that some of these responses may have reflected accidental button presses rather than transient perceptual capacities. For the 16 ms colorterm stimulusterm, five subjectsterm never responded, and detectionterm rates for the remaining six subjectsterm were as follows: 10, 15, 25, 30, 30, 40%. The average false alarm rate (responses to random stimuli at any of the five stimulusterm durations) was 0.5%. Three subjectsterm had 2% false alarm rates while all other subjectsterm had zero false alarms. All three subjectsterm showing false alarm rates > 0 also showed detectionterm rates > 0 for the 16 ms colorterm stimulusterm.

Figure 4.

Detectionterm rates as a function of masking SOAterm·var for shapeterm (square) and colorterm (4-red-lines) stimuli in the behavioral experiment . Error bars reflect the standard error of the mean (s.e.m.)term·stat.

Because our goal was to identify a single masking SOAterm·var that could render both shapeterm and colorterm stimuli invisible for a large majority of subjectsterm/trials, we chose the 16 ms SOA for use in the EEG experiment. Importantly, because roughly half of the subjectsterm in this behavioral experiment showed non-zero detectionterm rates for the 16 ms colorterm stimulusterm, we also administered a behavioral post-test after each EEG session (see methods above). We excluded from EEG analyses any subjectterm who responded to one or more 16 ms stimuli in this post-test (five out of 26 subjectsterm were excluded for this reason). For the remaining subjectsterm, detectionterm rates in this behavioral post-test were 0% for both 16 ms stimuli and 97.73% (s.e.m. = 0.18%) and 98.19% (s.e.m. = 0.10%) for the 300 ms shapeterm and colorterm stimuli, respectively.

EEG experiment Behavioral results from the EEG experiment indicated that the shapeterm task was slightly more difficult than the colorterm task, although performance on both tasks was strong. For the shapeterm task, subjectsterm detected the 300 ms diamond-shaped targets on 93.55% of trials (s.e.m. = 1.3%), d' = 4.61 (s.e.m. = 0.11), RT = 563 ms (s.e.m. = 10 ms). For the colorterm task, subjectsterm detected the 300 ms 3-red-line targets on 98.24% of trials (s.e.m. = 0.5%), d' = 4.68 (s.e.m. = 0.09), RT = 537 ms (s.e.m. = 10 ms). While d' did not differ statistically across the two tasks, RTs were significantly shorter for the colorterm task, t (18) = 4.56, p = 0.0003. Response rates to the 16 ms colorterm and 16 ms shapeterm targets were both 0%.

Grand-averaged ERPsterm elicited by the non-target shapeterm and colorterm stimuli are compared to ERPsterm elicited by the random (control) stimuli in Figures 5 , 6 , respectively. In both figures, electrodes representative of the scalp locations of the main components of interest are shown. Note that the ERPsterm elicited by the control stimuli differ according to stimulusterm duration and that within-block comparisons were made in all cases. For example, the shape-elicited ERPsterm in the aware, task-relevant condition were compared to the random-stimulus ERPsterm during the shape-task blocks, whereas the shape-elicited ERPsterm in the aware, task-irrelevant condition were compared to the random-stimulus ERPsterm during the color-task blocks. Difference waves formed by subtracting the ERPsterm to the appropriate control stimuli from the ERPsterm to the shapeterm and colorterm stimuli are shown in Figure 7 . In these difference waves the components CINterm (shapeterm) SEC (colorterm), VANterm, LOP, and P3bterm can be visualized. Results from all statistical analyses are provided below for shapeterm and colorterm stimuli, for each of the components of interest, organized according to their temporal sequence (see Methods Section for descriptions of each component's time course and scalp distribution).

Figure 5.

Grand-averaged ERPsterm elicited by shapeterm (square) and random (control) stimuli across the four main experimental conditions .

Figure 6.

Grand-averaged ERPsterm elicited by colorterm (4-red-lines) and random (control) stimuli across the four main experimental conditions .

Figure 7.

Grand-averaged difference waves for shapeterm stimuli (square minus random) and colorterm stimuli (4-red-lines minus random) across the four conditions of interest . Components are labeled at representative electrodes. CINterm, contour-integration negativity; SEC, sensory effect of colorterm·def; VANterm, visual awarenessterm negativity; LOP, late occipital positivity; P3bterm, centro-parietal positivity.

Early sensory effects ANOVAterm·stat for the CINterm component elicited by the outline square showed a main effect of awarenessterm, F (17) = 12.42 ( p = 0.0026), a main effect of task-relevanceterm, F (17) = 11.74 ( p = 0.0032), and no interaction. Cluster mass permutation analyses for each condition separately confirmed that these main effects were due to significant amplitudeterm differences in the aware, task-relevant (−1.58 μV, SD = 1.38) and aware, task-irrelevant (−0.91 μV, SD = 1.41) conditions (Figure S1 ). Difference amplitudesterm in the unaware, task-relevant and unware, task-irrelevant conditions did not significantly differ from zero; although a trend toward a negative difference over the posterior scalp was observed for the unaware, task-relevant conditions (see Figure 8 ).

Figure 8.

Grand-averaged difference wave topographies (square minus random) plotted over the posterior scalp for the four components of interest (columns) across the four main experimental conditions (rows) . Note that the amplitudeterm scale for the CINterm component was adjusted to ± 1 μV for the unaware conditions, and for the VANterm component ± 2 μV for all conditions except the aware, task-relevant condition. Asterisks indicate significant amplitudeterm differences ( p < 0.05) between shapeterm and random ERPterm as assessed via cluster mass permutation teststerm·stat for each condition separately.

ANOVAterm·stat for the SEC component elicited by the colored lines revealed a main of effect of awarenessterm, F (17) = 15.24 ( p = 0.0011), with no main effect of task-relevanceterm, nor an interaction between the two. Permutation analyses confirmed significant amplitudeterm differences in the aware, task-relevant (1.87 μV, SD = 2.16) and aware, task-irrelevant (0.83 μV, SD = 1.24) conditions, while amplitudeterm differences in both unaware conditions were not significant (Figure S2 ).

Visual awarenessterm negativity (VANterm) For the shape-elicited VANterm component, ANOVAterm·stat resulted in a main effect of awarenessterm, F (17) = 11.83 ( p = 0.0031), a main effect of task-relevanceterm, F (17) = 17.83 ( p = 0.00057), and a significant interaction, F (17) = 8.42 ( p = 0.0099). Cluster mass permutation teststerm·stat revealed a significant VANterm component in the aware, task-relevant and aware, task-irrelevant conditions and an absence of this component in both unaware conditions. The interaction between awarenessterm and task-relevanceterm was explained by a substantial amplitudeterm increase in the aware, task-relevant (−3.19 μV, SD = 3.09) compared to the aware, task-irrelevant condition (−1.58 μV, SD = 2.02).

ANOVAterm·stat for the color-elicited VANterm showed a main effect of awarenessterm, F (17) = 40.91 ( p = 0.000007), a main effect of task-relevanceterm, F (17) = 15.05 ( p = 0.0012), and an interaction between the two F (17) = 14.21 ( p = 0.0015). Similar to the shape-elicited VANterm, cluster permutation teststerm·stat showed significant amplitudeterm differences in both aware conditions and the interaction was explained by relatively larger amplitudesterm in the aware, task-relevant (−5.77 μV, SD = 3.91) vs. the aware , task-irrelevant condition (−3.56 μV, SD = 2.54) along with no significant differences in either of the unaware conditions.

Late positivites ANOVAterm·stat for the shape-elicited LOP component showed a main effect of awarenessterm, F (17) = 46.79 ( p = 0.000003), a main effect of task-relevanceterm, F (17) = 11.03 ( p = 0.0040), and a significant interaction, F (17) = 29.60 ( p = 0.000044). Permutation teststerm·stat suggested that these effects were due to a large amplitudeterm difference in the aware, task-relevant condition (4.48 μV, SD = 2.70), a smaller difference in the aware, task-irrelevant condition (1.48 μV, SD = 2.02), along with no significant amplitudeterm differences in either unaware condition.

For the color-elicited LOP, ANOVAterm·stat indicated a main effect of awarenessterm, F (17) = 15.67 ( p = 0.0010), a main effect of task-relevanceterm, F (17) = 35.41 ( p = 0.000016), and a significant interaction, F (17) = 25.05 ( p = 0.00011). However, unlike the shape-elicited LOP, cluster mass permutation teststerm·stat showed that these effects were driven by a large amplitudeterm difference in the aware, task-relevant condition (4.59 μV, SD = 3.48), along with a smaller effect in the unaware, task-relevant condition (0.67 μV, SD = 1.09). No amplitudeterm differences during the LOP time window were evident in the aware, task-irrelevant or unaware, task-irrelevant conditions.

Finally, for the P3bterm analyses, ANOVAterm·stat for the shapeterm stimuli resulted in a main effect of awarenessterm, F (17) = 26.67 ( p = 0.000078), a main effect of task-relevanceterm, F (17) = 18.51 ( p = 0.00048), and a significant interaction, F (17) = 36.85 ( p = 0.000012). All of these effects were driven by a large amplitudeterm difference in the aware, task-relevant condition (7.72 μV, SD = 5.85), along with no significant amplitudeterm effects in any of the other conditions. Although cluster permutation analyses showed positive amplitudeterm differences in the aware, task-irrelevant condition from ~300–400 ms (Figure S1 ), these effects correspond to the small LOP described above and were absent for electrode sites and time windows corresponding to the P3bterm.

ANOVAterm·stat for the P3bterm elicited by the colorterm stimuli also showed a main effect of awarenessterm, F (17) = 33.32 ( p = 0.000023), a main effect of task-relevanceterm, F (17) = 34.71 ( p = 0.000018), and a significant interaction, F (17) = 22.63 ( p = 0.00018). Cluster mass permutation teststerm·stat for each condition revealed a different pattern of effects from that of the shape-elicited P3bterm. In this case, color-elicited P3bterm amplitudesterm were significant for all conditions except the unaware, task-irrelevant condition. The P3bterm in the unaware, task-relevant condition (1.31 μV, SD = 1.43) was similar in magnitude to the P3bterm in the aware, task-irrelevant condition (1.73 μV, SD = 1.76) and occurred slightly earlier in time (see Figure S2 ), while the P3bterm in the aware, task-relevant condition was clearly the largest (8.28 μV, SD = 5.50).

Results summary Figures 8 , 9 provide summaries of the results for shapeterm and colorterm stimuli, respectively. In these figures, scalp topographies for each of the main components (defined by amplitudeterm differences between shapeterm and random ERPsterm, and colorterm and random ERPsterm, respectively) are provided across all four conditions resulting from the 2 × 2 manipulation of awarenessterm and task-relevanceterm. Asterisks under the scalp maps indicate that a significant amplitudeterm difference was found during the component's time-window as assessed by cluster mass permutation teststerm·stat.

Figure 9.

Grand-averaged difference wave topographies (4-red-lines minus random) plotted over the posterior scalp for the four components of interest (columns) across the four main experimental conditions (rows) . Note that the amplitudeterm scales for the SEC and LOP components were adjusted to ± 1 μV for the unaware conditions, and for the P3bterm component ± 2 μV for all conditions except the aware, task-relevant condition. Asterisks indicate significant amplitudeterm differences ( p < 0.05) between shapeterm and random ERPterm as assessed via cluster mass permutation teststerm·stat for each condition separately.

The overall goal of this experiment was to identify components that are present in both aware conditions (regardless of task-relevanceterm) and absent in both unaware conditions. Across the shapeterm and colorterm stimuli, only the early sensory components (CINterm, SEC) and the visual awarenessterm negativity (VANterm) showed this pattern. For both shapeterm and colorterm, these components were evident in aware conditions and absent in unaware conditions, regardless of task-relevanceterm. Whereas the LOP also showed this pattern for the shapeterm stimuli (Figure 8 ), it was absent for aware, task-irrelevant colorterm stimuli (Figure 9 ). The P3bterm did not consistently correlate with awarenessterm in shapeterm or colorterm trials (Figures 8 , 9 ), being absent for aware, task-irrelevant shapesterm, and present for unaware, task-relevant colorterm.

Discussion In agreement with previous results using the inattentional blindnessterm·mth paradigmterm·mth (PittspersName et al., 2012 , 2014 ), the present study used a 2 × 2 manipulation of awarenessterm and task-relevanceterm in a backward maskingterm·mth task and found a consistent ERPterm correlate of conscious visual perception, the visual awarenessterm negativity (VANterm) component. The VANterm is a mid-latency occipital-parietal negativity (measured here from 200 to 240 ms) that has been targeted by a number of previous studies using various awarenessterm manipulations (Koivisto and Revonsuo, 2003 , 2008 , 2010 ; Ojanen et al., 2003 ; Wilenius-Emet et al., 2004 ; Koivisto et al., 2005 ; Wilenius and Revonsuo, 2007 ; Railo et al., 2011 ; Sandberg et al., 2013 ). ERPterm components preceding the VANterm are likely to reflect pre-consciousterm processing, considering that a previous study using identical stimuli (PittspersName et al., 2012 ) found evidence for the elicitation of such components in unaware (and unmasked) conditions. In the current study, components prior to the VANterm were absent in the unaware conditions, suggesting interference of pre-consciousterm processing by the maskingterm·mth stimulusterm (presented at 16 ms SOA). Components subsequent to the VANterm have often been proposed as potential NCCsterm, including most notably the P3bterm component (Sergent et al., 2005 ; Babiloni et al., 2006 ; Del Cul et al., 2007 ; Lamy et al., 2009 ; Dehaene and Changeux, 2011 ; Batterink et al., 2012 ; Kouider et al., 2013 ). The current study, however, provides evidence against this view, as the P3bterm along with another component subsequent to the VANterm (the LOP) did not consistently correlate with awarenessterm. Instead, these later components are likely to reflect post-perceptualterm or attention-based processes necessary for completing the task, as their amplitudesterm were by far the largest in the aware/task-relevant condition. Moreover the P3bterm was present in some of the unaware, task-relevant conditions, and absent in some of the aware, task-irrelevant conditions.

Correlates of visual awarenessterm vs. post-perceptualterm processing It is difficult to create controlled conditions in which subjectsterm are aware vs. unaware of physically identical stimuli without requiring an immediate trial-by-trial perceptual reportterm·mth. Nevertheless, it is important to devise new methods for allowing such contrasts because the neural correlates of conscious perceptionterm are easily confusable with the neural correlates of post-perceptualterm maintenance and accessterm for immediate subjective reportterm·mth. In both task-relevant and task-irrelevant situations (in which the stimuli are readily visible), subjectsterm are considered to be conscious of the perceptual information because whenever they are asked to reportterm·mth what they see, they are able to easily do so. It follows that brain activity associated with conscious perceptionterm should be present in both cases. However, when perceptual information is accessed for immediate reportterm·mth, a variety of additional neural processes are likely to ensue, each of which is related to “doing something extra” with the perceptual information the subjectterm is already conscious of. Importantly, our manipulation of task-relevanceterm was designed to test a particular post-perceptualterm process: access of perceptual information for reportterm·def . This should not be confused with the more general concept of conscious accessterm (Dehaene and Changeux, 2004 ; Block, 2005 ), which we assume was present in our aware (300 ms stimulusterm) task- irrelevant conditions. In other words, we expect that on any given trial, if the subjectsterm had been asked, they would have easily been able to reportterm·mth seeing the 300 ms task-irrelevant stimuli (this was indirectly verified by our behavioral experiment and behavioral post-test), thus perceptual information was globally available but the subjectsterm did not have to use this information to complete the primary task-at-hand.

In our previous inattentional blindnessterm·mth experiments (PittspersName et al., 2012 , 2014 ; Shafto and PittspersName, 2013 ), we attempted to deal with this issue by rendering a stimulusterm easily visible (if expected) but irrelevant to the task-at-hand and delaying the perceptual reportterm·mth until after a full block of trials. In this situation, in which subjectsterm were fully aware of a stimulusterm but did not have to do anything with the perceptual information because it was irrelevant to the task, we found that only early sensory (CINterm) and mid-latency (VANterm) ERPterm components were elicited. Subsequent components such as the P3bterm were only evident when the stimuli became relevant to the task. In the current experiment, instead of diverting attentionterm to create an unaware condition, we severely masked some stimuli (16 ms masking SOAterm·var) and compared ERPsterm to conditions in which the same stimuli were clearly visible (300 ms masking SOAterm·var). Importantly, in order to assess post-perceptualterm processing we manipulated the task such that stimuli were relevant to the task during some blocks of trials and irrelevant during other blocks. We found a similar pattern of results as in the inattentional blindnessterm·mth studies, in that the VANterm was consistently associated with perceptual awarenessterm·def, while subsequent components were either absent when the stimuli were irrelevant to the task or present when subjectsterm were unaware of task-relevant stimuli.

Despite the main pattern of results, it remains possible that a small P3bterm was present (but below the statistical thresholdterm) during aware, task-irrelevant shapeterm trials (both in the current study as well as in PittspersName et al., 2012 and PittspersName et al., 2014 ). In this case, one might argue that the P3bterm is a correlate of conscious perceptionterm but was very weak during the task-irrelevant conditions because subjectsterm were so focused on the relevant stimuli that they only caught a glimpse of the irrelevant stimuli on a subset of trials. Future studies might address this by incorporating infrequent, unexpected, probe trials in which the experiment is interrupted after a task-irrelevant stimulusterm and subjectsterm are asked to “reportterm·mth what you just saw.” If subjectsterm can always reportterm·mth awarenessterm of task-irrelevant stimuli, but the P3bterm is still absent, a stronger case could be made for a lack of a relationship between the P3bterm and awarenessterm; however, one must be careful to avoid inadvertently rendering the task-irrelevant stimuli relevant by including too many “surprise” reportterm·mth trials.

Attentionterm in the absence of awarenessterm?

An unexpected finding in the current study was evidence for a P3bterm elicited in the absence of reported awarenessterm. This effect appeared in the unaware, task-relevant condition for colorterm stimuli. It was absent for the equivalent condition for shapeterm stimuli and there was no evidence for a P3bterm in any of the unaware, task-irrelevant conditions. While very few studies have reported a P3bterm in the absence of conscious perceptionterm, it is generally accepted that attentionterm and awarenessterm are independent (yet often interact), and there is growing evidence for attentional modulations in the absence of awarenessterm (Bernat et al., 2001 ; Koch and Tsuchiya, 2007 ; Wyart and Tallon-Baudry, 2008 ; Tsuchiya and Koch, 2009 ; Bachmann, 2011 ; Tallon-Baudry, 2011 ; Marchetti, 2012 ; Aru and Bachmann, 2013 ). We previously posited that the P3bterm is post-perceptualterm and argued that while the P3bterm does not appear to be necessary for conscious perceptionterm, it may be a sufficient marker; i.e., whenever a P3bterm is observed one can be confident that the subjectterm was aware of the stimulusterm (PittspersName et al., 2012 , 2014 ). The current result, however, suggests that the P3bterm might not be necessary or sufficient, as it was elicited by colorterm stimuli of which the subjectterm was presumably unaware. Interestingly, the P3bterm was completely absent for task-irrelevant colorterm stimuli of which the subjectterm was also unaware, thus suggesting a task-based attentional modulation of perceptually undetected stimuli. This result is consistent with a recent study that showed an N2pc component for colorterm singletons that captured attentionterm even when the subjectterm was unaware of the stimuli, but only when colorterm was relevant to the search task (Ansorge et al., 2010 ), as well as an earlier study that found evidence of attentionterm capture (N2pc) in the absence of awarenessterm due to object substitution maskingterm·mth (Woodman and Luck, 2003 ). Similarly, recent studies have provided evidence for working memoryterm related processing in the absence of awarenessterm (Hassin et al., 2009 ; Gilchrist and Cowan, 2010 ; Soto et al., 2011 ).

An alternative explanation for this finding is that some subjectsterm on some trials may have been partially aware of the 16 ms colorterm stimuli even though their reportsterm·mth indicated lack of awarenessterm. In these partial awarenessterm situations, subjectsterm may have attempted to perform the discrimination task (to determine if the stimulusterm contained 3 or 4 red lines) but could only detect the presence of colorterm without being able to discriminate between target and non-target colorterm stimuli (see Windey et al., 2014 for a recent review of graded vs. dichotomous awarenessterm). While we conducted an initial behavioral study to determine an appropriate masking SOAterm·var and administered a behavioral post-test to each of the EEG subjectsterm in which a simple detectionterm task replaced the discrimination task, it is still possible that some residual awarenessterm for a number of colorterm stimuli occurred during the EEG portion of the study. Indeed, we excluded five out of the original 26 participants because they were able to detect at least one of the 16 ms colorterm stimuli during the behavioral post-test. Because one of the goals of the current design was to avoid trial-by-trial reportsterm·mth, we intentionally did not acquire the data necessary to fully evaluate this alternative interpretation. Future studies should consider following up on this preliminary result in order to determine whether a P3bterm can be elicited during attentive, but unaware conditions, perhaps by employing a detectionterm task with low response criterion during EEG recording (Squires et al., 1973 , 1975 ).

Pre-consciousterm processing In contrast to our previous results using the inattentional blindnessterm·mth paradigmterm·mth (PittspersName et al., 2012 ), the current study provided no evidence for an early pre-consciousterm ERPterm difference between shapeterm and random stimuli in the unaware conditions. One of the major findings in our previous study was that a component we labeled as Nd1 (for negative difference 1, here referred to as the CINterm), distributed over the occipital midline from ~160–200 ms, was elicited in all conditions, even when subjectsterm were unaware of (inattentionally blind to) the shapeterm patterns. Why was this component absent from the unaware conditions in the current study? The most likely possibility is due to the differences in bottom-up stimulusterm strength between the two studies, a factor that is known to influence whether a stimulusterm will be processed non-consciously, pre-consciously, or consciously (Dehaene et al., 2006 ). In our previous inattentional blindnessterm·mth experiment, the shapeterm stimuli were always presented for 300 ms in duration (including the unaware condition), whereas the current study employed heavily masked stimuli (16 ms durations) to create the unaware conditions. In line with the interactions between top-down attentionterm and bottom-up stimulusterm strength described by Dehaene et al. ( 2006 ), the current results showed a small (just below statistical thresholdterm) CINterm in the unaware, task-relevant condition. In other words, with such severe maskingterm·mth and the resulting reduction of bottom-up stimulusterm strength, an unseen stimulusterm might only be processed pre-consciously if attended. In contrast, in our previous study top-down attentionterm was not required because sufficient bottom-up stimulusterm strength allowed this same stimulusterm to be processed pre-consciously.

One of the advantages of the current experimental design was a degree of internal replication made possible by the 2 × 2 crossing of the colorterm and shapeterm stimuli/tasks. This allows one to ask whether the same pattern of results seen for the shapeterm stimuli was also observed for the colorterm stimuli. An early sensory effect of colorterm·def (SEC) was not observed for either of the unaware conditions, although a trend in this direction was evident (see Figure 9 , left column, third row). To further explore how pre-consciousterm processing is influenced by top-down attentionterm and bottom-up stimulusterm strength, future studies could present extended duration colorterm stimuli during inattentional blindnessterm·mth or present backward-masked colorterm stimuli at various masking SOAsterm·var while manipulating task-relevanceterm.

VANterm: attentionterm or awarenessterm?

A main focus of recent consciousness research has been the relationship between attentionterm and awarenessterm (Tsuchiya and vanterm Boxtel, 2013 ). Historically, attentionterm and consciousness were often treated as similar if not identical concepts; nowadays, however, many researchers are proposing that each refers to a separate category of neural and psychological processes. Although attentionterm and awarenessterm may be functionally distinct, the question of whether each can exist independently of the other remains a topic of debate (Cohen et al., 2011 , 2012 ; Tsuchiya et al., 2012 ; Aru and Bachmann, 2013 ). One view posits that attentionterm can operate in the absence of awarenessterm, and awarenessterm can occur in the absence of attentionterm, whereas an opposing view argues that while attentionterm can influence processing of stimuli of which the subjectterm is unaware, there is no such thing as awarenessterm in the absence of attentionterm; i.e., attentionterm is necessary for conscious perceptionterm. Results from experiments employing the inattentional blindnessterm·mth paradigmterm·mth offer strong support for the latter view (Cohen et al., 2011 ; Mack and Clarke, 2012 ; PittspersName et al., 2012 ).

The present results, along with our previous inattentional blindnessterm·mth results, suggest that the most viable candidate for an ERPterm correlate of awarenessterm is the VANterm (Nd2) component. In our previous study (PittspersName et al., 2012 ), a well-known attention-related component, the SNterm (Harter and Aine, 1984 ; HillyardpersName and Anllo-Vento, 1998 ), was evident immediately after the VANterm, but was only observed in conditions where the stimulusterm was task-relevant. Distinguishing between the VANterm and the SNterm in a data-driven manner is not easy, because both components consist of a mid-latency (~200–300 ms), posterior, bi-lateral negativity. To further complicate matters, both the VANterm and the SNterm show variable (and overlapping) latencies depending on the stimuli and task. The only way to isolate the VANterm from the SNterm component may be to manipulate task-relevanceterm; in our previous study both components were present in task-relevant situations, whereas only the VANterm was present in aware but task-irrelevant conditions (PittspersName et al., 2012 ). In the present study, however, no clear SNterm was evident in the aware, task-relevant condition, perhaps because the stimuli used here were so easily discriminable that the processing resources indexed by the SNterm did not have to be engaged. Alternatively, it is possible that the VANterm measured in the current study overlapped the SNterm in the task-relevant condition such that the two components were indistinguishable. It will be important for future studies to distinguish between the VANterm and the SNterm, especially in situations in which the stimuli are task-relevant.

In the current study as well as in PittspersName et al. ( 2012 ), the amplitudeterm of the VANterm was larger in the task-relevant compared to the task-irrelevant condition. If the VANterm indeed reflects perceptual awarenessterm·def, which is often assumed to be an all-or-none phenomenon (you see the stimulusterm or you don't), why might its amplitudeterm vary according to the task? One possibility might be that subjectsterm were not aware of the task-irrelevant 300 ms stimuli on every single trial because their attentionterm was focused on a separate task (i.e., partial inattentional blindnessterm·mth). This seems unlikely, especially for the colorterm stimuli (see Movie 1 ); in a separate experiment (PittspersName et al., 2014 ) we found a 0% inattentional blindnessterm·mth rate for similar 300 ms colorterm stimuli. Another possibility is that the timing of perceptual awarenessterm·def is more consistent across trials when the stimulusterm is relevant to the task; whereas, on task-irrelevant trials subjectsterm may notice the irrelevant stimuli on every trial but at slightly different times on different trials because their primary task is to determine if a potential target is present. If this is the case, one would expect larger amplitudesterm with briefer time-courses for awareness-related ERPsterm in task-relevant conditions and smaller amplitudesterm with extended durations for the same ERPterm components in task-irrelevant conditions, given that the ERPsterm are derived by averaging across many trials. Data from PittspersName et al. ( 2012 ) follow this pattern very closely, and although the current data show amplitudeterm differences for the VANterm without obvious corresponding differences in component duration, the shapeterm of the VANterm is slightly skewed with a longer right-tail in the task-irrelevant condition (see Figure 7 ), consistent with the trial-by-trial latencyterm jitter account. A third alternative explanation is that the VANterm and SNterm components may have been temporally superimposed such that only a portion of this negativity reflects perceptual awarenessterm·def. The amplitudeterm increase during task-relevant situations might be due to an increase in top-down attentionterm reflected by the SNterm component, rather than a larger number of aware trials or greater trial-to-trial consistency in the timing of awarenessterm.

While there is growing evidence that the VANterm tracks closely with awarenessterm while the SNterm varies as a function of task demands and attentionterm, it is important to acknowledge the existence of a variety of attentional processes. In addition to exogenous (bottom-up) and endogenous (top-down) attentionterm, visual attentionterm can be selectively allocated to spatial locations, features, or entire objects. An alternative interpretation of the VANterm is that it reflects some form of object-basedterm attentionterm that is necessary for conscious perceptionterm (perhaps a specific interaction between attentionterm and high-level perceptual representations). Because many manipulations of awarenessterm also involve manipulations of attentionterm, this possibility cannot be easily discounted. To give some examples, inattentional blindnessterm·mth involves altering attentionterm to alter awarenessterm; backward maskingterm·mth at short vs. long latencies alters bottom-up attentionterm to influence awarenessterm; backward maskingterm·mth and signal detectionterm at thresholdterm capitalizes on stochastic trial-by-trial fluctuations of attentionterm; the attentional blink involves differences in attentionterm between seen and unseen stimuli; and change blindness differs from change detectionterm based on the allocation of spatial attentionterm·var. Because of the common co-manipulation of attentionterm and awarenessterm across a variety of paradigmsterm·mth, we previously argued that naming an ERPterm component the “visual awarenessterm negativity” (VANterm) might be pre-mature (PittspersName et al., 2012 ), although we adopt this nomenclature here for consistency with the literature. If the VANterm turns out to reflect a type of object-basedterm attentionterm instead of awarenessterm per se , this might suggest that an obvious ERPterm correlate of conscious perceptionterm has yet to be discovered (Verleger, 2010 ). This would explain the amplitudeterm increase for the VANterm in task-relevant vs. task-irrelevant conditions, i.e., task-relevanceterm enhances object-basedterm attentionterm. Importantly, this would not mean that a neural correlate of awarenessterm does not exist, but rather that ERPsterm can only measure a limited set of neuronal events. In any case, studies of ERPsterm can still be useful in helping to narrow down the time-window for which potential NCCsterm could be found, while more sensitive techniques such as intra-cranial recordings in human epileptic patients may be necessary to identify NCCsterm.

A final possibility worth consideration is whether a particular type of interaction between attentionterm and perceptual representation is the underlying neural mechanism of conscious awarenessterm, and the VANterm is a marker of this type of interaction. To explore this idea, future consciousness research might focus efforts on understanding object-basedterm attentionterm, perceptual encoding, and the interaction between the two, rather than searching for neurons or neural networks specifically dedicated to consciousness per se (Cohen and Dennett, 2011 ). Currently, there is not strong evidence for or against the view that the VANterm component reflects object-basedterm attentionterm instead of visual awarenessterm. In addition to developing experimental paradigmsterm·mth which can better isolate NCC-proper from pre-consciousterm and post-perceptualterm activity (the focus of the current special issue), it is imperative that researchers craft experimental designs that improve our chances of distinguishing between neural correlates of object-basedterm attentionterm and neural correlates of awarenessterm.

Conflict of interest statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments The authors would like to thank the reviewers for their insightful comments, especially regarding alternative approaches to data analysis. We would also like to thank Michael Cohen for constructive comments on earlier drafts of this manuscript, and Enriqueta Canseco-Gonzalez for fruitful discussions regarding statistical analyses.

Supplementary material The Supplementary Material for this article can be found online at: http://www.frontiersin.org/journal/10.3389/fpsyg.2014.01078/abstract Movie 1 Video depicting an example sequence of trials from the EEG experiment (instructions refer to a block of trials in which shapesterm were task-relevant) .

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