How can we incentivize Post-Publication Peer Review?

Open review of “Post-Publication Peer Review for Real”
by Koki Ikeda, Yuki Yamada, and Kohske Takahashi (pp2020)

[I7R8]

Our system of pre-publication peer review is a relict of the age when the only way to disseminate scientific papers was through print media. Back then the peer evaluation of a new scientific paper had to precede its publication, because printing (on actual paper if you can believe it) and distributing the physical print copies is expensive. Only a small selection of papers could be made accessible to the entire community.

Now the web enables us to make any paper instantly accessible to the community at negligible cost. However, we’re still largely stuck with pre-publication peer review, despite its inherent limitations: to a small number of preselected reviewers who operate in isolation from and without the scrutiny of the community.

People familiar with the web who have considered, from first principles, how a scientific peer review system should be designed tend to agree that it’s better to make a new paper publicly available first, so the community can take note of the work and a broader set of opinions can contribute to the evaluation. Post-publication peer review also enables us to make the evaluation transparent: Peer reviews can be open responses to a new paper. Transparency promises to improve reviewers’ motivation to be objective, especially if they choose to sign and take responsibility for their reviews.

We’re still using the language of a bygone age, whose connotations make it hard to see the future clearly:

  • A paper today is no longer made of paper — but let’s stick with this one.
  • A preprint is not something that necessarily precedes the publication in print media. A better term would be “published paper”.
  • The term publication is often used to refer to a journal publication. However, preprints now constitute the primary publications. First, a preprint is published in the real sense: the sense of having been made publicly available. This is in contrast to a paper in Nature, say, which is locked behind a paywall, and thus not quite actually published. Second, the preprint is the primary publication in that it precedes the later appearance of the paper in a journal.

Scientists are now free to use the arXiv and other repositories (including bioRxiv and PsyArXiv) to publish papers instantly. In the near future, peer review could be an open and open-ended process. Of course papers could still be revised and might then need to be re-evaluated. Depending on the course of the peer evaluation process, a paper might become more visible within its field, and perhaps even to a broader community. One way this could happen is through its appearance in a journal.

The idea of post-publication peer review has been around for decades. Visions for open post-publication peer review have been published. Journals and conferences have experimented with variants of open and post-publication peer review. However, the idea has yet to revolutionize the scientific publication system.

In their new paper entitled “Post-publication Peer Review for Real”, Ikeda, Yamada, and Takahashi (pp2020) argue that the lack of progress with post-publication peer review reflects a lack of motivation among scientists to participate. They then present a proposal to incentivize post-publication peer review by making reviews citable publications published in a journal. Their proposal has the following features:

  • Any scientist can submit a peer review on any paper within the scope of the journal that publishes the peer reviews (the target paper could be published either as a preprint or in any journal).
  • Peer reviews undergo editorial oversight to ensure they conform to some basic requirements.
  • All reviews for a target paper are published together in an appealing and readable format.
  • Each review is a citable publication with a digital object identifier (DOI). This provides a new incentive to contribute as a peer reviewer.
  • The reviews are to be published as a new section of an existing “journal with high transparency”.

Ikeda at al.’s key point that peer reviews should be citable publications is solid. This is important both to provide an incentive to contribute and also to properly integrate peer reviews into the crystallized record of science. Making peer reviews citable publications would be a transformative and potentially revolutionary step.

The authors are inspired by the model of Behavioral and Brain Sciences (BBS), an important journal that publishes theoretical and integrative perspective and review papers as target articles, together with open peer commentary. The “open” commentary in BBS is very successful, in part because it is quite carefully curated by editors (at the cost of making it arguably less than entirely “open” by modern standards).

BBS was founded by Stevan Harnad, an early visionary and reformer of scientific publishing and peer review. Harnad remained editor-in-chief of BBS until 2002. He explored in his writings what he called “scholarly skywriting“, imagining a scientific publication system that combines elements of what is now known as open-notebook science and research blogging with preprints, novel forms of peer review, and post-publication peer commentary.

If I remember correctly, Harnad drew a bold line between peer review (a pre-publication activity intended to help authors improve and editors select papers) and peer commentary (a post-publication activity intended to evaluate the overall perspective or conclusion of a paper in the context of the literature).

I am with Ikeda et al. in believing that the lines between peer review and peer commentary ought to be blurred. Once we accept that peer review must be post-publication and part of a process of community evaluation of new papers, the prepublication stage of peer review falls away. A peer review, then, becomes a letter to both the community and to the authors and can serve any combination of a broader set of functions:

  • to explain the paper to a broader audience or to an audience in an adjacent field,
  • to critique the paper at the technical and conceptual level and possibly question its conclusions,
  • to relate it to the literature,
  • to discuss its implications,
  • to help the authors improve the paper in revision by adding experiments or analyses and improving the exposition of the argument in text and figures.

An example of this new form is the peer review you are reading now. I review only papers that have preprints and publish my peer reviews on this blog. This review is intended for both the authors and the community. The authors’ public posting of a preprint indicates that they are ready for a public response.

Admittedly, there is a tension between explaining the key points of the paper (which is essential for the community, but not for the authors) and giving specific feedback on particular aspects of the writing and figures (which can help the authors improve the paper, but may not be of interest to the broader community). However, it is easy to relegate detailed suggestions to the final section, which anyone looking only to understand the big picture can choose to skip.

Importantly, the reviewer’s judgment of the argument presented and how the paper relates to the literature is of central interest to both the authors and the community. Detailed technical criticism may not be of interest to every member of the community, but is critical to the evaluation of the claims of a paper. It should be public to provide transparency and will be scrutinized by some in the community if the paper gains high visibility.

A deeper point is that a peer review should speak to the community and to the authors in the same voice: in a constructive and critical voice that attempts to make sense of the argument and to understand its implications and limitations. There is something right, then, about merging peer review and peer commentary.

While reading Ikeda et al.’s review of the evidence that scientists lack motivation to engage in post-publication peer review, I asked myself what motivates me to do it. Open peer review enables me to:

  • more deeply engage the papers I review and connect them to my own ideas and to the literature,
  • more broadly explore the implications of the papers I review and start bigger conversations in the community about important topics I care about,
  • have more legitimate power (the power of a compelling argument publicly presented in response to the claims publicly presented in a published paper),
  • have less illegitimate power (the power of anonymous judgment in a secretive process that decides about publication of someone else’s work)
  • take responsiblity for my critical judgments by subjecting them to public scrutiny
  • make progress with my own process of scientific insight
  • help envision a new form of peer review that could prove positively transformative

In sum, open post-publication peer review, to me, is an inherently more meaningful activity than closed pre-publication peer review. I think there is plenty of motivation for open post-publication peer review, once people overcome their initial uneasiness about going transparent. A broader discussion of researcher motivations for contributing to open post-publication peer review is here.

That said, citability and DOIs are essential, and so are the collating and readability of the peer reviews of a target paper. I hope Ikeda et al. will pursue their idea of publishing open post-publication peer reviews in a journal. Gradually, and then suddenly, we’ll find our way toward a better system.

 

Suggestions for improvements

(1) The proposal raises some tricky questions that the authors might want to address:

  • Which existing “journal with high transparency” should this be implemented in?
  • Should it really be a section in an existing journal or a new journal (e.g. the “Journal of Peer Reviews in Psychology”)?
  • Are the peer reviews published immediately as they come in, or in bulk once there is a critical mass?
  • Are new reviews of a target paper to be added on an ongoing basis in perpetuity?
  • How are the target papers to be selected? Should their status as preprints or journal publications make any difference?
  • Why do we need to stick with the journal model? Couldn’t commentary sections on preprint servers solve the problem more efficiently — if they were reinvented to provide each review also as a separate PDF with beautiful and professional layout, along with figure and LaTeX support and, critically, citability and DOIs?

Consider addressing some of these questions to make the proposal more compelling. In particular, it seems attractive to find an efficient solution linked to preprint servers to cover large parts of the literature. Can the need for editorial work be minimized and the critical incentive provided through beautiful layout, citability, and DOIs?

 

(2) Cite and and discuss some of Stevan Harnad’s contributions. Some of the ideas in this edited collection of visions for post-publication peer review may also be relevant.

 


A recent large-scale survey reported that 98% of researchers who participated in the study agreed that the peer-review system was important (or extremely important) to ensure the quality and integrity of science. In addition, 78.8% answered that they were satisfied (or very satisfied) with the current review system (Publon, 2018) . It is probably true that peer-review has been playing a significant role to control the quality of academic papers (Armstrong, 1997) . The latter result, however, is rather perplexing, since it has been well known that sometimes articles could pass through the system without their flaws being revealed (Hopewell et al., 2014) , results could not be
reproduced reliably (e.g. Open Science Collaboration, 2015) , decisions were said to be no better than a dice roll (Lindsey, 1988; Neff & Olden, 2006) , and inter-reviewer agreement was estimated to be very low (Bornmann et al., 2010).

(3) Consider disentangling the important pieces of evidence in the above passage a little more. “Perplexing” seems the wrong word here: Peer review can be simultaneously the best way to evaluate papers and imperfect. It would be good to separate mere evidence that mistakes happen (which appears unavoidable), from the stronger criticism that peer review is no better than random evaluations. A bit more detail on the cited results suggesting it is no better than random would be useful. Is this really a credible conclusion? Does it require qualifications?

 

The low reliability across reviewers is especially disturbing and raises serious concerns about the effectiveness of the system, because we now have empirical data showing that inter-rater agreement and precision could be very high, and they robustly predict the replicability of previous studies, when the information about others’ predictions are shared among predictors (Botvinik-Nezer et al., 2020; Camerer et al., 2016, 2018; Dreber et al., 2015; Forsell et al., 2019) . Thus, the secretiveness of the current system could be the unintended culprit of its suboptimality.

(4) Consider revising the above passage. Inter-reviewer agreement is an important metric to consider. However, even zero correlation between reviewer’s ratings does not imply that the reviews are random. Reviewers may focus on different criteria. For example, if one reviewer judged primarily the statistical justification of the claims and another primarily the quality of the writing, the correlation between their ratings could be zero. However, the average rating would be a useful indicator of quality. Averaging ratings in this context does not serve merely to reduce the noise in the evaluations, it also serves to compromise between different weightings of the criteria of quality.

Interaction among reviewers that enables them to adjust their judgments can fundamentally enhance the review process. However, inter-rater agreement is an ambiguous measure, when the ratings are not independent.

 

However, BBS commentary is different from them in terms of that it employs an “open” system so that anyone can submit the commentary proposal at will (although some commenters are arbitrarily chosen by the editor). This characteristic makes BBS commentary much more similar to PPPR than other traditional publications.

(5) Consider revising. Although BBS commentaries are nothing like traditional papers (typically much briefer statements of perspective on a target paper) and are a form of post-publication evaluation, they are also very distinct in form and content. I think Stevan Harnad made this point somewhere.

 

Next and most importantly, the majority of researchers find no problem with their incentives to submit an article as a BBS commentary, because they will be considered by many researchers and institutes to be equivalent to a genuine publication and can be listed on one’s CV. Therefore, researchers have strong incentives to actively publish their reviews on BBS .

(6) Consider revising. It’s a citable publication, yes. However, it’s in a minor category, nowhere near a primary research paper or a full review or perspective paper.

 

There seem to be at least two reasons for this uniqueness. Firstly, BBS is undoubtedly one of the most prestigious journals in psychology and its
related areas, with a 17.194 impact factor for the year 2018. Secondly, the commentaries are selected by the editor before publication, so their quality is guaranteed at least to some extent. Critically, no current PPPR has the features comparable to these in BBS.

(7) Consider revising. While this is true for BBS, I don’t see how a journal of peer reviews that is open to all articles within a field, including preprints, as the target papers could replicate the prestige of BBS. This passage doesn’t seem to help the argument in favor of the new system as currently proposed. However, you might revise the proposal. For example, I could imagine a “Journal of Peer Commentary in Psychology” applying the BBS model to editorially selected papers of broad interest.

 

To summarize, we might be able to create a new and better PPPR system by simply combining the advantages of BBS commentary – (1) strong incentive for commenters and (2) high readability – with those of the current PPPRs – (3) unlimited target selection and (4) unlimited commentary accumulation -. In the next section, we propose a possible blueprint for the implementation of these ideas, especially with a focus on the first two, because the rest has already been realized in the current media.

(8) Consider revising. The first two points seem at a strong tension with the second two points. Strong incentive to review requires highly visible target publications, which isn’t possible if target selection is unlimited. High readability also appears compromised when reviews come in over a long period and there is no limit to their number. This should at least be discussed.

Among the features that seem critical to the successful implementation of PPPR, strong incentives for commenters is probably the most important factor. We speculated that BBS has achieved this goal by providing the commentaries a status equivalent to a standard academic paper. Furthermore, this is probably realized by the journal’s two unique characteristics: its academic prestige and the selection of commentaries by the editor. Based on these considerations, we propose the following plans for the new PPPR system.

(9) Consider revising. As discussed above, the commentaries do not quite have “equivalent” status to a standard academic paper.

 

The four pillars of open science

An open review of Gorgolewski & Poldrack (PP2016)

the 4 pillars of open science.png

The four pillars of open science are open data, open code, open papers (open access), and open reviews (open evaluation). A practical guide to the first three of these is provided by Gorgolewski & Poldrack (PP2016). In this open review, I suggest a major revision in which the authors add treatment of the essential fourth pillar: open review. Image: The Porch of the Caryatids (Porch of the Maidens) of the ancient Greek temple Erechtheion on the north side of the Acropolis of Athens.

 

Open science is a major buzz word. Is all the talk about it just hype? Or is there a substantial vision that has a chance of becoming a reality? Many of us feel that science can be made more efficient, more reliable, and more creative through a more open flow of information within the scientific community and beyond. The internet provides the technological basis for implementing open science. However, making real progress with this positive vision requires us to reinvent much of our culture and technology. We should not expect this to be easy or quick. It might take a decade or two. However, the arguments for openness are compelling and open science will prevail eventually.

The major barriers to progress are not technological, but psychological, cultural, and political: individual habits, institutional inertia, unhealthy incentives, and vested interests. The biggest challenge is the fact that the present way of doing science does work (albeit suboptimally) and our vision for open science has not merely not yet been implemented, but has yet to be fully conceived. We will need to find ways to gradually evolve our individual workflows and our scientific culture.

Gorgolewski & Poldrack (PP2016) offer a brief practical guide to open science for researchers in brain imaging. I was expecting a commentary reiterating the arguments for open science most of us have heard before. However, the paper instead makes good on its promise to provide a practical guide for brain imaging and it contains many pointers that I will share with my lab and likely refer to in the future.

The paper discusses open data, open code, and open publications – describing tools and standards that can help make science more transparent and efficient. My main criticism is that it leaves out what I think of as a fourth essential pillar of open science: open peer review. Below I first summarise some of the main points and pointers to resources that I took from the paper. Along the way, I add some further points overlooked in the paper that I feel deserve consideration. In the final section, I address the fourth pillar: open review. In the spirit of a practical guide, I suggest what each of us can easily do now to help open up the review process.

 

1 Open data

  • Open-data papers more cited, more correct: If data for a paper are published, the community can reanalyse the data to confirm results and to address additional questions. Papers with open data are cited more (Piwowar et al. 2007, Piwowar & Vision 2013) and tend to make more correct use of statistics (Wicherts et al. 2011).
  • Participant consent: Deidentified data can be freely shared without consent from the participants in the US. However, rules differ in other countries. Ideally, participants should consent to their data being shared. Template text for consent forms is offered by the authors.
  • Data description: The Brain Imaging Data Structure (BIDS) (Gorgolewski et al. 2015) provides a standard (evolved from the authors’ OpenfMRI project; Poldrack et al. 2013) for file naming and folder organisation, using file formats such as NifTI, TSV and JSON.
  • Field-specific brain-imaging data repositories: Two repositories accept brain imaging data from any researcher: FCP/INDI (for resting state fMRI only) and OpenfMRI (for any datasets that includes MRI data).
  • Field-general repositories: Field-specific repositories like those mentioned help standardise sharing for particular types of data. If the formats offered are not appropriate for the data to be shared, field-general repositories, including FigShare, Dryad, or DataVerse can be used.
  • Data papers: A data paper is a paper that focusses on the description of a particular data set that is publicly accessible. This helps create incentives for ambitious data acquisitions and to enable researchers to specialise in data acquisition. Journals publishing data papers include: Scientific Data, Gigascience, Data in Brief, F1000Research, Neuroinformatics, and Frontiers in Neuroscience.
  • Processed-data sharing: It can be useful to share intermediate or final results of data analysis. With the initial (and often somewhat more standardised) steps of data processing out of the way, processed data are often much smaller in volume and more immediately amenable to further analyses by others. Statistical brain-imaging maps can be shared via the authors’ NeuroVault.org website.

 

2 Open code

  • Code sharing for transparency and reuse: Data-analysis details are complex in brain imaging, often specific to a particular study, and seldom fully defined in the methods section. Sharing code is the only realistic way of fully defining how the data have been analysed and enabling others to check the correctness of the code and effects of adjustments. In addition, the code can be used as a starting point for the development of further analyses.
  • Your code is good enough to share: A barrier to sharing is the perception among authors that their code might not be good enough. It might be incompletely documented, suboptimal, or even contain errors. Until the field finds ways to incentivise greater investment in code development and documentation for sharing, it is important to lower the barriers to sharing. Sharing imperfect code is preferable to not sharing code (Barnes 2010).
  • Sharing does not imply provision of user support: Sharing one’s code does not imply that one will be available to provide support to users. Websites like org can help users ask and answer questions independently (or with only occasional involvement) of the authors.
  • Version Control System (VCS) essential to code sharing: VCS software enables maintenance of complex code bases with multiple programmers and versions, including the ability to merge independent developments, revert to previous versions when a change causes errors, and to share code among collaborators or publicly. An excellent, freely accessible, widely used, web-based VCS platform is com, introduced in Blischak et al. (2016).
  • Literate programming combines code and results and text narrative: Scripted automatic analyses have the advantage of automaticity and reproducibility (Cusack et al. 2014), compared to point-and-click analysis in an application with a graphical user interface. However, the latter enables more interactive interrogation of the data. Literate programming (Knuth 1992) attempts to make coding more interactive and provides a full and integrated record of the code, results, and text explanations. This provides a fully computationally transparent presentation of results, makes the code accessible to oneself later in time, and to collaborators and third parties, with whom literate programs can be shared (e.g. via GitHub). Software supporting this includes: Jupyter (for R, Python and Julia), R Markdown (for R) and matlabweb (for MATLAB).

 

3 Open papers

  • Open notebook science: Open science is about enhancing the bandwidth and reducing the latency in our communication network. This means sharing more and at earlier stages, not only our data and code, but ultimately also our day-to-day incremental progress. This is called open notebook science and has been explored, by Cameron Neylon and Michael Nielson among others. Gorgolewski & Poldrack don’t comment on this beautiful vision for an entirely different workflow and culture at all. Perhaps open notebook science is too far in the future? However, some are already practicing it. Surely, we should start exploring it in theory and considering what aspects of open notebook science we can integrate into our workflow. It would be great to have some pointers to practices and tools that help us move in this direction.
  • The scientific paper remains a critical component of scientific communication: Data and code sharing are essential, but will not replace communication through permanently citable scientific papers that link (increasingly accessible) data through analyses to novel insights and relate these insights to the literature.
  • Papers should simultaneously achieve clarity and transparency: The conceptual clarity of the argument leading to an insight is often at a tension with the transparency of all the methodological details. Ideally, a paper will achieve both clarity and transparency, providing multiple levels of description: a main narrative that abstracts from the details, more detailed descriptions in the methods section, additional detail in the supplementary information, and full detail in the links to the open data and code, which together enable exact reproduction of the results in the figures. This is an ideal to aspire to. I wonder if any paper in our field has fully achieved it. If there is one, it should surely be cited.
  • Open access: Papers need to be openly accessible, so their insights can have the greatest positive impact on science and society. This is really a no brainer. The internet has greatly lowered the cost of publication, but the publishing industry has found ways to charge higher prices through a combination of paywalls and unreasonable open-access charges. I would add that every journal contains unique content, so the publishing industry runs hundreds of thousands of little monopolies – safe from competition. Many funding bodies require that studies they funded be published with open access. We need political initiatives that simply require all publicly funded research to be publicly accessible. In addition, we need publicly funded publication platforms that provide cost-effective alternatives to private publishing companies for editorial boards that run journals. Many journals are currently run by scientists whose salaries are funded by academic institutions and the public, but whose editorial work contributes to the profits of private publishers. In historical retrospect, future generations will marvel at the genius of an industry that managed for decades to employ a community without payment, take the fruits of their labour, and sell them back to that very community at exorbitant prices – or perhaps they will just note the idiocy of that community for playing along with this racket.
  • Preprint servers provide open access for free: Preprint servers like bioRxiv and arXiv host papers before and after peer review. Publishing each paper on a preprint server ensures immediate and permanent open access.
  • Preprints have digital object identifiers (DOIs) and are citable: Unlike blog posts and other more fleeting forms of publication, preprints can thus be cited with assurance of permanent accessibility. In my lab, we cite preprints we believe to be of high quality even before peer review.
  • Preprint posting enables community feedback and can help establish precedence: If a paper is accessible before it is finalised the community can respond to it and help catch errors and improve the final version. In addition, it can help the authors establish the precedence of their work. I would add that this potential advantage will be weighed against the risk of getting scooped by a competitor who benefits from the preprint and is first to publish a peer-reviewed journal version. Incentives are shifting and will encourage earlier and earlier posting. In my lab, we typically post at the time of initial submission. At this point getting scooped is unlikely, and the benefits of getting earlier feedback, catching errors, and bringing the work to the attention of the community outweighs any risks of early posting.
  • Almost all journals support the posting of preprints: Although this is not widely known in the brain imaging and neuroscience communities, almost all major journals (including Nature, Science, Nature Neuroscience and most others) have preprint policies supportive of posting preprints. Gorgolewski & Poldrack note that they “are not aware of any neuroscience journals that do not allow authors to deposit preprints before submission, although some journals such as Neuron and Current Biology consider each submission independently and thus one should contact the editor prior to submission.” I would add that this reflects the fact that preprints are also advantageous to journals: They help catch errors and get the reception process and citation of the paper going earlier, boosting citations in the two-year window that matters for a journal’s impact factor.

 

4 Open reviews

The fourth pillar of open science is the open evaluation (OE, i.e. open peer review and rating) of scientific papers. This pillar is entirely overlooked in the present version of the Gorgolewski & Poldrack’s commentary. However, peer review is an essential component of communication in science. Peer review is the process by which we prioritise the literature, guiding each field’s attention, and steering scientific progress. Like other components of science, peer review is currently compromised by a lack of transparency, by inefficiency of information flow, and by unhealthy incentives. The movement for opening the peer review process is growing.

In traditional peer review, we judge anonymously, making inherently subjective decisions that decide about the publication of our competitors’ work, under a cloak of secrecy and without ever having to answer for our judgments. It is easy to see that this does not provide ideal incentives for objectivity and constructive criticism. We’ve inherited secret peer review from the pre-internet age (when perhaps it made sense). Now we need to overcome this dysfunctional system. However, we’ve grown used to it and may be somewhat comfortable with it.

Transparent review means (1) that reviews are public communications and (2) that many of them are signed by their authors. Anonymous reviewing must remain an option, to enable scientists to avoid social consequences of negative judgments in certain scenarios. However, if our judgment is sound and constructively communicated, we should be able to stand by it. Just like in other domains, transparency is the antidote to corruption. Self-serving arguments won’t fly in open reviewing, and even less so when the review is signed. Signing adds weight to a review. The reviewer’s reputation is on the line, creating a strong incentive to be objective, to avoid any impression of self-serving judgment, and to attempt to be on the right side of history in one’s judgment of another scientist’s work. Signing also enables the reviewer to take credit for the hard work of reviewing.

The arguments for OE and a synopsis of 18 visions for how OE might be implemented are given in Kriegeskorte, Walther & Deca (2012). As for other components of open science, the primary obstacles to more open practices are not technological, but psychological, cultural, and political. Important journals like eLife and those of the PLoS family are experimenting with steps toward opening the review process. New journals including, the Winnower, ScienceOpen, and F1000 Research already rely on postpublication peer review.

We don’t have to wait for journals to lead us. We have all the tools to reinvent the culture of peer review. The question is whether we can handle the challenges this poses. Here, in the spirit of Gorgolewki & Poldrack’s practical guide, are some ways that we can make progress toward OE now by doing things a little differently.

  • Sign peer reviews you author: Signing our reviews is a major step out of the dark ages of peer review. It’s easier said than done. How can we be as critical as we sometimes have to be and stand by our judgment? We can focus first on the strengths of a paper, then communicate all our critical arguments in a constructive manner. Some people feel that we must sign either all or none of our reviews. I think that position is unwise. It discourages beginning to sign and thus de facto cements the status quo. In addition, there are cases where the option to remain anonymous is needed, and as long as this option exists we cannot enforce signing anyway. What we can do is take anonymous comments with a grain of salt and give greater credence to signed reviews. It is better to sign sometimes than never. When I started to sign my reviews, I initially reserved the right to anonymity for myself. After all this was a unilateral act of openness; most of my peers do not sign their reviews. However, after a while, I decided to sign all of my reviews, including negative ones.
  • Openly review papers that have preprints: When we read important papers as preprints, let’s consider reviewing them openly. This can simultaneously serve our own and our collective thought process: an open notebook distilling the meaning of a paper, why its claims might or might not be reliable, how it relates to the literature, and what future steps it suggests. I use a blog. Alternatively or additionally, we can use PubMed Commons or PubPeer.
  • Make the reviews you write for journals open: When we are invited to do a review, we can check if the paper has been posted as a preprint. If not, we can contact the authors, asking them to consider posting. At the time of initial submission, the benefits tend to outweigh the risks of posting, so many authors will be open to this. Preprint posting is essential to open review. If a preprint is available, we can openly review it immediately and make the same review available to the journal to contribute to their decision process.
  • Reinvent peer review: What is an open review? For example, what is this thing you’re reading? A blog post? A peer review? Open notes on the essential points I would like to remember from the paper with my own ideas interwoven? All of the above. Ideally, an open review helps the reviewer, the authors, and the community think – by explaining the meaning of a paper in the context of the literature, judging the reliability of its claims, and suggesting future improvements. As we begin to review openly, we are reinventing peer review and the evaluation of scientific papers.
  • Invent peer rating: Eventually we will need quantitative measures evaluating papers. These should not be based on buzz and usage statistics, but reflect the careful judgement of peers who are experts in the field, have considered the paper in detail, and ideally stand by their judgment. Quantitative judgments can be captured in ratings. Multidimensional peer ratings can be used to build a plurality of paper evaluation functions (Kriegeskorte 2012) that prioritise the literature from different perspectives. We need to invent suitable rating systems. For primary research papers, I use single-digit ratings on multiple scales including reliability, importance, and novelty, using capital letters to indicate the scale in the following format: [R7I5].

 

Errors are normal

As we open our science and share more of it with the community, we run the risk of revealing more of our errors. From an idealistic perspective that’s a good thing, enabling us learn more efficiently as individuals and as a community. However, in the current game of high-impact biomedical science there is an implicit pretense that major errors are unlikely. This is the reason why, in the rare case that a major error is revealed despite our lack of transparent practices, the current culture requires that everyone act surprised and the author be humiliated. Open science will teach us to drop these pretenses. We need to learn to own our mistakes (Marder 2015) and to be protective of others when errors are revealed. Opening science is an exciting creative challenge at many levels. It’s about reinventing our culture to optimise our collective cognitive process. What could be more important or glamorous?

 

Additional suggestions for improvements in revision

  • A major relevant development regarding open science in the brain imaging community is the OHBM’s Committee on Best Practices in Data Analysis and Sharing (COBIDAS), of which author Russ Poldrack and I are members. COBIDAS is attempting to define recommended practices for the neuroimaging community and has begun a broad dialogue with the community of researchers (see weblink above). It would be good to explain how COBIDAS fits in with the other developments.
  • About a third of the cited papers are by the authors. This illustrates their substantial contribution and expertise in this field. I found all these papers worthy of citation in this context. However, I wonder if other groups that have made important contributions to this field should be more broadly cited. I haven’t followed this literature closely enough to give specific suggestions, but perhaps it’s worth considering whether references should be added to important work by others.
  • As for the papers, the authors are directly involved in most of the cited web resources OpenfMRI, NeuroVault, NeuroStars.org. This is absolutely wonderful, and it might just be that there is not much else out there. Perhaps readers of this open review can leave pointers in the comments in case they are aware of other relevant resources. I would share these with the authors, so they can consider whether to include them in revision.
  • Can the practical pointers be distilled into a table or figure that summarises the essentials? This would be a useful thing to print out and post next to our screens.
  • “more than fair” -> “only fair”

 

Disclosures

I have the following relationships with the authors.

relationship number of authors
acquainted 2
collaborated on committee 1
collaborated on scientific project 0

 

References

Barnes N (2010) Publish your computer code: it is good enough. Nature. 467: 753. doi: 10.1038/467753a

Blischak JD, Davenport ER, Wilson G. (2016) A Quick Introduction to Version Control with Git and GitHub. PLoS Comput Biol. 12: e1004668. doi: 10.1371/journal.pcbi.1004668

Cusack R, Vicente-Grabovetsky A, Mitchell DJ, Wild CJ, Auer T, Linke AC, et al. (2014) Automatic analysis (aa): efficient neuroimaging workflows and parallel processing using Matlab and XML. Front Neuroinform. 2014;8: 90. doi: 10.3389/fninf.2014.00090

Gorgolewski KJ, Auer T, Calhoun VD, Cameron Craddock R, Das S, Duff EP, et al. (2015) The Brain Imaging Data Structure: a standard for organizing and describing outputs of neuroimaging experiments [Internet]. bioRxiv. 2015. p. 034561. doi: 10.1101/034561

Gorgolewski KJ, Varoquaux G, Rivera G, Schwarz Y, Ghosh SS, Maumet C, et al. (2015) NeuroVault.org: a webbased repository for collecting and sharing unthresholded statistical maps of the human brain. Front Neuroinform. Frontiers. 9. doi: 10.3389/fninf.2015.00008

Knuth DE (1992) Literate programming. CSLI Lecture Notes, Stanford, CA: Center for the Study of Language and Information (CSLI).

Kriegeskorte N, Walther A, Deca D (2012) An emerging consensus for open evaluation: 18 visions for the future of scientific publishing Front. Comput. Neurosci http://dx.doi.org/10.3389/fncom.2012.00094

Kriegeskorte N (2012) Open evaluation: a vision for entirely transparent post-publication peer review and rating for science. Front. Comput. Neurosci., 17 http://dx.doi.org/10.3389/fncom.2012.00079

Marder E (2015) Living Science: Owning your mistakes DOI: http://dx.doi.org/10.7554/eLife.11628 eLife 2015;4:e11628

Piwowar HA, Day RS, Fridsma DB (2007) Sharing detailed research data is associated with increased citation rate. PLoS One. 2007;2: e308. doi: 10.1371/journal.pone.0000308

Piwowar HA, Vision TJ (2013) Data reuse and the open data citation advantage. PeerJ. 1: e175. doi: 10.7717/peerj.175

Poldrack RA, Barch DM, Mitchell JP, Wager TD, Wagner AD, Devlin JT, et al. (2013) Toward open sharing of taskbased fMRI data: the OpenfMRI project. Front Neuroinform. 2013;7: 1–12. doi: 10.3389/fninf.2013.00012

Wicherts JM, Bakker M, Molenaar D (2011) Willingness to Share Research Data Is Related to the Strength of the Evidence and the Quality of Reporting of Statistical Results. Tractenberg RE, editor. PLoS One. 6: e26828. doi: 10.1371/journal.pone.0026828

 

 

 

 

 

 

 

 

Imagining and seeing objects elicits consistent category-average activity patterns in the ventral stream

[R8I7]

Horikawa and Kamitani report results of a conceptually beautiful and technically sophisticated study decoding the category of imagined objects. They trained linear models to decode visual image features from fMRI voxel patterns. The visual features are computed from images by computational models including GIST and the AlexNet deep convolutional neural net. AlexNet provides features spanning the range from visual to semantic. A subject is then scanned while imagining images from a novel object category (not used in training the fMRI decoder). The decoder is used to predict the computational-model representation for the imagined category (averaged across exemplars of that category). This predicted model representation is then compared to the actual model representation for many categories, including the imagined one. The model representation predicted from fMRI during imagery is shown to be significantly more similar to the model representation of images from the imagined category than to the model representation of images from other categories.

ScreenShot685

Figure from Horikawa & Kamitani (2015)

The methods are sophisticated and will give experts much to think about and draw from in developing better decoders. Comprehensive supplementary analyses, which I did not have time to fully review, complement and extend the thorough analyses provided. This is a great study. As usual in our field, a difficult question is what exactly it means for brain computational theory.

A few results that might speak to the computational mechanism of the ventral stream are as follows.

When predicting computational features of *single images* (which was only done for seen, not for imagined objects):

  • Lower layers of AlexNet are better predicted from voxels in lower ventral-stream areas.
  • Higher layers of AlexNet are better predicted from voxels in higher ventral-stream areas.
  • GIST features are best predicted from V1-3, but also significantly from higher areas.

This is consistent with the recent findings (Yamins, Khaligh-Razavi, Cadieu, Guclu) showing that deep convolutional neural nets explain lower- and higher-level ventral-stream areas with a rough correspondence of lower model layers to lower brain areas and higher model layers to higher brain areas. It is also consistent with previous findings that GIST, like many visual feature models, explains significant representational variance even in the higher ventral-stream representation (Khaligh-Razavi, Rice), but does not reach the noise ceiling (indicating that a data set is fully explained), as deep neural net models do (Khaligh-Razavi).

When predicting *category-averages* of computational features (which was done for seen and imagined objects):

  • Higher-level visual areas better predict features in all layers of AlexNet.
  • Higher layers of AlexNet are better predicted from voxels in all visual areas.

This is confusing, until we remember that it is category averages that are being predicted. Category averaging will retain a major portion of the representational variance of category-sensitive higher-level representations, while reducing the representational variance of low-level representations that are less related to categories. This may boost both predictions from category-related visual areas, as well as predictions of category-related model features.

Subjects imagined many different images from a given category in an experimental block during fMRI. The category-average imagery activity of the voxels was then used to predict the corresponding category-averages of the computational-model features. As expected, category-average computational-feature prediction is worse for mental imagery than for perception. The pattern across visual areas and AlexNet layers is similar for imagery and perception, with higher predictions resulting when the predicting visual area is category-related and when the predicted model feature is category-related. However, V1 and V2 did not consistently enable imagery decoding into the format of any of the layers of AlexNet. Interestingly, computational features more related to categories were better decodable. This supports the view that higher ventral-stream features might be optimised to emphasise categorical divisions (cf Jozwik et al. 2015).

 

Suggested improvements

(1) Clarify any evidence about the representational format in which the imagined content is represented. The authors’ model predicts both visual and semantic features of imagined object categories. This suggests that imagery involves both semantic and visual representations. However, the evidence for lower- or even mid-level visual representation of imagined objects is not very compelling here, because the imagery was not restricted to particular images. Instead the category-average imagery activity was measured. Each category is, of course, associated with particular visual features to some extent. We therefore expect to be able to predict category-average visual features from category-average voxel patterns better than chance. A strong claim that imagery paints low-level visual features into early visual representations would require imagery of particular images within each category. For relevant evidence, see Naselaris et al. (2015).

(2) Go beyond the decoding spin: what do we learn about computations in the ventral stream? Being able to decode brain representations is cool because it demonstrates unambiguously that a certain kind of information is present in a brain region. It’s even cooler to be able to decode into an open space of features or categories and to decode internally generated representations as done here. Nevertheless, the approach of decoding is also scientifically limiting. From the present version of the paper, the message I take is summarised in the title of the review: “Imagining and seeing objects elicits consistent category-average activity patterns in the ventral stream”. This has been shown previously (e.g. Stokes, Lee), but is greatly generalised here and is a finding so important that it is good to have it replicated and generalised in multiple studies. The reason why I can’t currently take a stronger computational claim from the paper is that we already know that category-related activity patterns cluster hierarchically in the ventral stream (Kriegeskorte et al. 2008) and may be continuously and smoothly related to a semantic space (Mitchell et al. 2008; Huth et al. 2012). In the context of these two pieces of knowledge, consistent category-average activity for perception and imagery is all that is needed to explain the present findings of decodability of novel imagined categories. The challenge to the authors: Can you test specific computational hypotheses and show something more on the basis of this impressive experiment? The semantic space analysis goes in this direction, but did not appear to me to support totally novel theoretical conclusions.

(3) Why decode computational features? Decoding of imagined content could be achieved either by predicting measured activity patterns from model representations of the stimuli (e.g. Kay et al. 2008) or by predicting model representations  from measured activity patterns (the present approach). The former approach is motivated by the idea that the model should predict the data and lends itself to comparing multiple models, thus contributing to computational theory. We will see below that the latter approach (chosen here) is less well suited to comparing alternative computational models. Why did Horikawa & Kamitani choose this approach? One argument might be that there are many model features and predicting the smaller number of voxels from these many features requires strong prior assumptions (implicit to regularisation), which might be questionable. The reverse prediction from voxels to features requires estimating the same total number of weights (# voxels * # model features), but each univariate linear model predicting a feature only has # voxels (i.e. typically fewer than # features) weights. Is this why you preferred this approach? Does it outperform the voxel-RF modelling approach of Kay et al. (2008) for decoding?

An even more important question is what we can learn about brain computations from feature decoding. If V4, say, perfectly predicted CNN1, this would suggest that V4 contains features similar to those in CNN1. However, it might additionally contain more complex features unrelated to CNN1. CNN1 predictability from V4, thus, would not imply that CNN1 can account for V4. Another example: CNN8 and GIST features are similarly predictable from voxel data across brain areas, and most predictable from V4 voxels. Does this mean GIST is as good a model as CNN8 for explaining the computational mechanism of the ventral stream? No. Even if the ventral-stream voxels perfectly predicted GIST, this would not imply that GIST perfectly predicts the ventral-stream voxels.

The important theoretical question is what computational mechanism gives rise to the representation in each area. For the human inferior temporal cortex, Khaligh-Razavi & Kriegeskorte (2015) showed that both GIST and the CNN representation explain significant variance. However, the GIST representation leaves a large portion of the explainable variance unexplained, whereas the CNN fully explains the explainable variance.

(4) Further explore the nature of the semantic space. To understand what drives the decoding of imagined categories, it would be helpful to see the performance of simpler analyses. Following Mitchell et al. (2008), one could use a text-corpus based semantic embedding to represent each of the categories. Decoding into this semantic embedding would similarly enable novel seen and imagined test categories (not used in training) to be decoded. It would be interesting, then, to successively reduce the dimensionality of the semantic embedding to estimate the complexity of the semantic space underlying the decoding. Alternatively, the authors’ WordNet distance could be used for decoding.

(5) Clarify that category-average patterns were used. The terms “image-based information” and “object-based information” are not ideal. By “image-based”, you are referring to a low-level visual representation and by “object-based”, to a categorical representation. Similarly, in many places where you say “objects” (as in “decoding objects”) it would be clearer to say “object categories”. Use clearer language throughout to clarify when it was category-average patterns that were used for prediction (brain representations) and that were predicted (model representations). This concerns the text and the figures. For example, the title of Fig. 4 should be: “Object-category-average feature decoding”. If this detracts the casual reader too lazy to even read the legends too much, at least the text of the legend should clearly state that category-average brain activity patterns are used to predict category-average model features.

(6) What are the assumptions implicit to sparse linear regression and is this approach optimal? L2 regularisation would spread the weights out over more voxels and might benefit from averaging out the noise component. Please comment on this choice and on any alternative performance results you may have.

 

Minor points

(7) The work is related to Mitchell et al. (2008), who predicted semantic semantic brain representations of novel stimuli using a semantic space model. This paper should be cited.

(8) “These studies showed a high representational similarity between the top layer of a convolutional neural network and visual cortical activity in the inferior temporal (IT) cortex of humans [24,25] and non-human primates [22,23].”

Ref 24 showed this for both human fMRI and macaque cell-recording data.

(9) “Interestingly, mid-level features were the most useful in identifying object categories, suggesting the significant contributions of mid-level representations in accurate object identification.”

This sentence repeats the same point after “suggesting”.