A neural representation of invisibility: when stimulus-specific neural activity negatively correlates with conscious experience

  1. Matthew J Davidson
  2. Will Mithen
  3. Hinze Hogendoorn
  4. Jeroen J.A. van Boxtel
  5. Naotsugu Tsuchiya

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Abstract

Although visual awareness of an object typically increases neural responses, we identify a neural response that increases prior to perceptual disappearances , and that scales with the amount of invisibility reported during perceptual filling-in. These findings challenge long-held assumptions regarding the neural correlates of consciousness and entrained visually evoked potentials, by showing that the strength of stimulus-specific neural activity can encode the conscious absence of a stimulus.

Significance Statement

The focus of attention and the contents of consciousness frequently overlap. Yet what happens if this common correlation is broken? To test this, we asked human participants to attend and report on the invisibility of four visual objects which seemed to disappear, yet actually remained on screen. We found that neural activity increased, rather than decreased, when targets became invisible. This coincided with measures of attention that also increased when stimuli disappeared. Together, our data support recent suggestions that attention and conscious perception are distinct and separable. In our experiment, neural measures more strongly follow attention.

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  1. eLife

    ###Reviewer #2:

    Overall, I think this is a creative study, with very interesting findings. A major weakness is that the interpretations seem a bit exaggerated and alternative interpretations not considered.

    Using a creative paradigm of perceptual filling-in, the authors show that increased attention (indexed by a reduction in alpha power over central-parietal locations, and supported by previous psychophysics studies) is associated with perceptual filling-in, and the phenomenal disappearance of targets. By tagging targets and surround with different frequencies, they show that SSVEP elicited by targets increases at the time of perceptual filling-in.

    These results suggest that SSVEP, thought to index the content of visual perception in previous binocular rivalry studies, can be dissociated from conscious perception in this paradigm, and instead reflect attention.

    While the results are interesting and novel, they are perhaps not as surprising as the authors present them to be. Given that previous studies have shown a clear connection between SSVEP and attention (e.g. Ref 14 cited by the authors), these results show that when attention and awareness are dissociated (as the last author has nicely demonstrated/argued previously), SSVEP goes with attention.

    These results do not demonstrate that all sensory-cortical activity goes along with attention instead of awareness, as the authors' abstract/significance statement/discussion suggest to be the case. E.g., in the abstract/significance statement, the authors only state "neural activity" or "neural response", instead of specifically SSVEP, which can be misleading. Similarly, in discussion, it remains a possibility that other types of neural activity (e.g. spiking rate or recurrent activity) in sensory cortex correlates with the vividness of conscious experience, which would in principle be consistent with first-order or GNW theories.

    An analysis comment:

    In discussion, the authors mention "As more targets disappeared and presumably drew attention, both the duration of their absence and strength of target SNR increased."

    The duration effect, shown in SI, is not referenced in the main text as I could find. In Fig. 2, in addition to investigating SSVEP's relation with the number of disappeared targets, the authors could also test its relation with the duration of PFI.

  2. eLife

    ###Reviewer #1:

    General assessment:

    In this paper, Davidson et al. characterize the neural correlates of visual disappearance during perceptual filling-in (PFI) using steady-state visual evoked potentials (SSVEPs). They show that target disappearance actually leads to an increase rather than to a decrease of the target SNR. This finding is potentially of importance. However, the current version of the manuscript does not provide enough details regarding the underlying assumptions and neural mechanisms. The results should also be better described, interpreted and compared to the existing literature. I list my most substantive concerns below.

    Substantive concerns:

    1. I was a bit frustrated to see that almost no discussion about the neural mechanisms underlying the results is provided. It seems important to better explain the cortical processes involved (e.g. the authors could compare more carefully their results with those obtained in macaque electrophysiology by De Weerd et al. 1995).

    To go further along this direction, one possibility would also be to analyse the SNRs at the intermodulation frequencies (I see in supplementary figure 3 that responses at F2-F1 = 5Hz are significantly above noise). This would permit to characterize and discuss the interactions between the neural responses corresponding to the processing of the targets and to the surround (see e.g. Appelbaum et al., 2008).

    1. When I read the whole manuscript, I had the feeling that the analysis of the SNR change latencies (which is currently described in the supplements) would deserve to be more documented and to appear in the main document. The finding that changes in background SNR precede changes in target SNR is an important result which clarifies the temporal sequence of neural activations. That would also be nice if the authors could determine when the SNR change corresponding to the inter-modulation product (e.g. at F2-F1) appears (see my first point above).

    2. To better characterize the difference between the responses to PFI vs to phenomenally matched disappearances (PMD) and support the claim that target-SNR decreases rather than increases during PMD (l. 170), that would be great to show the target-SNR changes around button press (i.e. the equivalent of figure 2 b & e) for PMD.

    3. The target disappearance during PFI is associated with an increase of SNR and therefore, SSVEPs in this case do not reflect conscious perception. But does it necessarily imply that this target-SNR increase reflects attention instead? The authors base their interpretation on previous studies (Lou, 1999; De Weerd et al., 2006) where attending to target feature increased PFI probability (which I think is not exactly equivalent to the PFI magnitude reported here) and also on the correlation they found between target-SNR and evoked alpha. However, these are indirect evidences and in their experimental protocol, attention was not directly manipulated (as e.g. in Morgan et al., 1996 or Müller et al., 2006). I would suggest being a little bit more cautious with this interpretation in the manuscript.

    4. Before this study, other groups looked at the dissociation between attention and perceptual awareness (among others, see e.g. Wyart & Tallon-Baudry, 2008; 2009; Koivisto et al., 2009; Norman et al., 2013). A deeper review of the existing literature on this topic (in the introduction and/or discussion) would permit to better understand what is already known and also to provide leads for future investigations.

  3. eLife

    ##Preprint Review

    This preprint was reviewed using eLife’s Preprint Review service, which provides public peer reviews of manuscripts posted on bioRxiv for the benefit of the authors, readers, potential readers, and others interested in our assessment of the work. This review applies only to version 2 of the manuscript.

    This manuscript is in revision at eLife.

    ###Summary:

    This manuscript describes a human EEG study which aims at characterizing the neural correlates of visual disappearance during perceptual filling-in (PFI) using steady-state visual evoked potentials (SSVEP). The authors report that target disappearance leads in this paradigm to an increase rather than to a decreased SNR of the target SSVEP. The authors interpret this "neural correlate of invisibility" as an empirical challenge for existing theories regarding the relationship between SSVEP and conscious perception. The two reviewers have found the study to be creative and its findings to be of potential importance for the field. However, they have also raised concerns regarding the interpretation of the findings proposed by the authors, which would require additional analyses to be supported by the data and a more extensive account of the existing literature on the relationship between the neural correlates of visual awareness and attention. There are also concerns regarding the number of subjects included in the analyses which should be clarified. The paragraphs below describe the main concerns that have been discussed among reviewers and the reviewing editor.

  5. Version published to 10.1101/2020.04.20.051334 on bioRxiv