Differential Effects of Awareness and Task Relevance on Early and Late Erps in a No-Report Visual Oddball Paradigm
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Research Articles: Behavioral/Cognitive Differential effects of awareness and task relevance on early and late ERPs in a no-report visual oddball paradigm https://doi.org/10.1523/JNEUROSCI.2077-19.2020 Cite as: J. Neurosci 2020; 10.1523/JNEUROSCI.2077-19.2020 Received: 28 August 2019 Revised: 9 December 2019 Accepted: 13 January 2020 This Early Release article has been peer-reviewed and accepted, but has not been through the composition and copyediting processes. The final version may differ slightly in style or formatting and will contain links to any extended data. Alerts: Sign up at www.jneurosci.org/alerts to receive customized email alerts when the fully formatted version of this article is published. Copyright © 2020 the authors The Journal of Neuroscience https://jneurosci.msubmit.net JN-RM-2077-19R1 Differential effects of awareness and task relevance on early and late ERPs in a no-report visual oddball paradigm Insa Schlossmacher, University of Muenster Torge Dellert, University of Muenster Michael Pitts, Reed College Maximilian Bruchmann, University of Muenster Thomas Straube, University Hospital Muenster Commercial Interest: This is a confidential document and must not be discussed with others, forwarded in any form, or posted on websites without the express written consent of The Journal for Neuroscience. 1 Differential effects of awareness and task relevance on early and late ERPs in a no- 2 report visual oddball paradigm 3 Abbreviated title: Deviance processing during inattentional blindness 4 5 Insa Schlossmacher1,2, Torge Dellert1,2, Michael Pitts3, Maximilian Bruchmann1,2, and 6 Thomas Straube1,2 7 8 1Institute of Medical Psychology and Systems Neuroscience, University of Münster, 48149 9 Münster, Germany 10 2Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Münster, 11 48149 Münster, Germany 12 3Department of Psychology, Reed College, Portland, OR 97202, USA 13 14 15 Corresponding author: 16 Insa Schlossmacher 17 E-mail: [email protected] 18 19 Manuscript summary: 20 Number of pages: 26 21 Number of Figures: 4 22 Number of Tables: 2 23 Number of Words: 24 Abstract: 209 25 Introduction: 635 26 Discussion: 1498 27 28 29 The authors declare no competing financial interests. 30 We thank Karen Vestring and Julia Krömer for their assistance in data collection. 31 1 32 Abstract 33 To date it is poorly understood how and when deviance processing interacts with awareness 34 and task relevance. Furthermore, an important issue in the study of consciousness is the 35 prevalent confound of conscious perception with the requirement of reporting it. This study 36 addresses these topics using a no-report inattentional blindness paradigm with a visual oddball 37 sequence of geometrical shapes presented to male and female human participants. 38 Electrophysiological responses were obtained in three physically identical phases A, B and C 39 that differed only with respect to the instructions: (A) participants were uninformed about the 40 shapes and attended an unrelated foreground task (inattentional blind), (B) were informed 41 about the shapes but still attended the foreground task and (C) attended the shapes. Conscious 42 processing of shapes was indexed by the visual awareness negativity (VAN) but not a P3. 43 Deviance processing was associated with the visual mismatch negativity (vMMN) 44 independently of consciousness and task relevance. The oddball P3, however, only emerged 45 when the stimuli were task relevant, and was absent for consciously perceived but task 46 irrelevant stimuli. The P3 thus does not represent a reliable marker of stimulus awareness. 47 This result pattern supports the view of hierarchical predictive processing, where lower levels 48 display automatic deviance processing, while higher levels require attention and task 49 relevance. 50 Significance Statement 51 In order to react to potentially important changes in our environment it is fundamental to 52 detect deviations from regularities of sensory input. It has yet to be understood how 53 awareness and task relevance of this input interact with deviance processing. We investigated 54 the role of awareness in deviance detection while at the same time circumventing the 55 confound of awareness and report by means of a no-report paradigm. Our results suggest that 56 early processes are elicited automatically while – contrary to prominent theories – late 2 57 processes do not depend on awareness but on task-based attention. 3 58 Introduction 59 The detection of deviations from regularities of sensory input is of fundamental 60 importance for reacting to – potentially important – changes in our environment. However, 61 the ways in which awareness and task relevance influence deviance processing are to date 62 poorly understood as both factors are often closely intertwined. Inattentional blindness (IB) 63 coupled with task manipulations can help disentangle these factors (Mack, 2003; Pitts et al., 64 2012; Shafto and Pitts, 2015). Besides being highly ecologically valid, the IB design of Pitts 65 and colleagues circumvents the need for trial-by-trial subjective reports (Pitts et al., 2018). 66 The confound of subjective report with conscious perception is a caveat often encountered in 67 consciousness research (Aru et al., 2012; Frässle et al., 2014; Tsuchiya et al., 2015; Pitts et al., 68 2018). As a result, brain activity related to awareness might be confused with brain activity 69 related to the report (Pitts et al., 2014; Tsuchiya et al., 2015). During no-report paradigms, a 70 negative-going potential at posterior sites indexed stimulus awareness (visual awareness 71 negativity (VAN); Koivisto and Revonsuo, 2010; Pitts et al., 2012; Shafto and Pitts, 2015; 72 Schelonka et al., 2017). This contrasts with findings postulating late central positivities (P3) 73 as a neural correlate of consciousness (NCC; Dehaene et al., 2006, 2014). However, this issue 74 is still hotly debated and warrants further studies corroborating the evidence of the few 75 existing no-report studies (Boly et al., 2017; Odegaard et al., 2017). 76 While the above-mentioned studies demonstrated the viability of IB in disentangling 77 report and awareness, the question of whether (and if so, how and when) complex mental 78 operations like deviance processing can be observed nonconsciously during IB has yet to be 79 addressed. Deviance processing is often probed using an oddball paradigm, in which the 80 expectation of a standard stimulus is violated by an unexpected deviant stimulus. In event- 81 related potentials (ERPs), such regularity violations by deviant stimuli are accompanied by an 82 early negativity termed the mismatch negativity (MMN; Näätänen et al., 2007; Stefanics et 4 83 al., 2014) and a later positivity (oddball P3; Squires et al., 1975; Snyder and Hillyard, 1976; 84 Conroy and Polich, 2007; Polich, 2007, 2012). ERP components in oddball studies have been 85 linked to the concept of predictive processing (Mars et al., 2008; Lieder et al., 2013; Stefanics 86 et al., 2014, 2018). In this framework, it is postulated that the brain processes information by 87 comparing top-down predictions with incoming data resulting in a prediction error signal 88 being passed on to the next higher level, thus enabling efficient information transmission 89 (Friston, 2010; Clark, 2013). Observing the MMN and oddball P3 under different awareness 90 and task conditions could highlight in what ways these components might represent correlates 91 of a hierarchical comparison process and strengthen the account of predictive processing as a 92 basic principle of information transmission in the brain. 93 While there is evidence for a nonconscious MMN, the P3 to deviant stimuli seems to 94 be elicited only during conscious processing (Faugeras et al., 2012; Strauss et al., 2015; Jack 95 et al., 2017; Bekinschtein et al., 2009; but see Silverstein et al., 2015). This outcome accords 96 with the proposal that awareness and the emergence of a P3 are strongly associated (Dehaene 97 et al., 2006, 2014). However, as discussed above, findings from no-report paradigms (Pitts et 98 al., 2012; Shafto and Pitts, 2015; Schelonka et al., 2017) leave open the possibility that 99 oddball effects on the P3 might not only depend on awareness, but on task-based attention. 100 Thus, the current study aimed to elucidate how deviance processing interacts with awareness 101 and task relevance using a roving oddball paradigm and a no-report procedure. We found the 102 VAN to index awareness and, together with the behavioral data, to validate the IB paradigm. 103 Crucially, we observed the MMN independently of awareness and task, while the oddball P3 104 only emerged in participants aware of the stimuli and only if the stimuli were task relevant. 105 Methods 106 Participants 107 The sample consisted of 56 participants (39 female) aged from 19 to 33 years 5 108 (M = 23.54, SD = 3.00). All had normal or corrected-to-normal vision and three were left- 109 handed. Participants volunteered and were compensated with 9 € per hour. Before starting, 110 participants were given written instructions on the experimental task and given the 111 opportunity to ask further questions. The study was approved by the local ethics committee 112 and all procedures were carried out in accordance with the Helsinki declaration. 113 Apparatus 114 The experiment was run using MATLAB and the Psychophysics Toolbox (Brainard, 115 1997; Pelli, 1997; Kleiner et al., 2007). An iiyama HM903DT monitor at 85 Hz with a 116 resolution of 1280 × 1024 pixels was employed for stimulus display. The viewing distance 117 amounted to 60 cm. To respond, participants pressed the space bar and numeric keys of a 118 standard keyboard. A chin rest was used to prevent head movements during the experiment. 119 Stimulus material and experimental procedure 120 Stimuli consisted of a 20 × 20 grid of white lines with a width of 0.45 degrees of 121 visual angle (°) each, spanning 10° × 10° in total and were presented on a black background 2 2 122 (Lwhite = 0.22 cd/m , Lblack = 181.34 cd/m ; for background stimuli, see Figure 1A).