PONE-D-21-22350

Predictive language comprehension in Parkinson’s disease

PLOS ONE

Dear Dr. Roberts,

Thank you for submitting your manuscript to PLOS ONE. I have now received reviews from 2 experts in the field and read your manuscript myself. We feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Both reviewers recommend additional analyses and clarification or elaboration on certain points. Their comments are quite clear and constructive, so I won’t reiterate them. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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We look forward to receiving your revised manuscript.

Kind regards,

Daniel Mirman

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: No

Reviewer #2: No

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: No

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The study investigated the capacity of patients with Parkinson’s disease to anticipate the object of sentences by measuring fixations in a visual-world paradigm. Patients with Parkinson’s disease did not show different patterns of fixation on the target (object) during sentence processing. There were differences between patients and controls for a small set of high motion verbs.

I am not surprised by the results. The analysis focused on the onset and increase of target fixation over time. However, the target was already cued by the agent (first noun) and later constrained by the verb. So, fixations on the target could be due in large part to its semantic relationship with the agent, and this aspect of language processing is well preserved in PD. This issue is not corrected by eliminating trials in which participants were already looking at the target at the beginning of the trial. Although I appreciate the authors’ rationale, it would be preferable to report the results with all trials, at least in supplementary materials. Authors should report analyses comparing the time taken by participants to stop looking at the agent distractor once the verb was presented. This word is still compatible with the agent, but disengagement from the agent distractor would be expected if people predicted the next word based on verb information. Focusing the analysis on the agent distractor and/or on a proportion between agent distractor and target fixations could be more informative. Authors might find this paper interesting:

Hochstadt, J. (2009). Set-shifting and the on-line processing of relative clauses in Parkinson's disease: Results from a novel eye-tracking method. Cortex, 45(8), 991-1011.

I provide detailed comments below.

Introduction

less commonly, outright dementia = dementia is not common at disease onset, but it is common when patients are followed longitudinally

Hely, M. A., Reid, W. G., Adena, M. A., Halliday, G. M., & Morris, J. G. (2008). The Sydney multicenter study of Parkinson's disease: the inevitability of dementia at 20 years. Movement disorders, 23(6), 837-844.

Cardona et al. proposed that action-language networks involve not only motor cortex and respective mirror neuron systems but also cortical-subcortical systems. = Expand the review of papers showing the involvement of mirror neurons and motor areas for verbs and action language processing.

If event knowledge deficits are a symptom of Parkinson’s disease, then cognitively intact participants with Parkinson’s disease may show impaired processing of verbs and of their event-based semantic associates, compared to healthy adults. Online language processing may be particularly challenging for people with PD, considering that healthy adults activate event knowledge both to process and to predict language as it unfolds in real time. = This hypothesis is interesting, but it is not clear how experimental manipulations can help distinguish between event knowledge, verb semantics (motion content, lexical aspect-telicity, etc.), thematic roles, etc. This should be clarified or acknowledged as a limitation.

Under Huettig’s account, deficits in the use of verb specific thematic fit information in PD would appear capable of disrupting the proper functioning of multiple language prediction mechanisms. = The argument made in this sentence appears somewhat circular. PD patients can’t use thematic information for language predictions because processing of thematic information is impaired. Rephrase or clarify.

Relatively few published studies have investigated predictive processing based on thematic fit in cognitively intact participants with PD. = The term “cognitively intact” is charged and full of implications. Speaking of participants who do not have self-reported and measurable signs of cognitive decline might be more appropriate (see Litvan et al. 2012 for discussion on the criteria for MCI in PD and lack of consensus on how they should be applied).

Thus, what remains unclear is whether language prediction deficits appear in PD in situations that require rapid integration of concepts for combinatorial processing, as in combining agent-based and verb-based sources of semantic information. = How to integrate the results of studies on lexical activation delay in PD into this question?

We hypothesized that because people with PD evince impairments in action and event semantic knowledge, they should show impaired online processing of sentences that require rapidly combining thematic fit information from an agent noun and a verb to predict the post-verb object (patient). = I don’t think the word “require” is appropriate in this context, since participants are not made aware of the real purpose of the task. They are never “required” to fixate the target as rapidly as possible (or at all).

Although attention, working memory, and executive function impairments have sometimes been implicated in language processing impairments in PD, the objective of the present study was to investigate combinatorial semantic language prediction abilities in a cohort without concomitant cognitive impairment. = Same issue as above. No reported and measurable signs of cognitive impairment would be preferable.

Aim 1 examined whether the inability to integrate multiple sources of thematic role

information, grounded in deficits in event knowledge, is a source of language impairment in PD. = Please provide more support and citations for 1) the idea that thematic roles are related to event knowledge and 2) the idea that event knowledge (script memory?) is impaired in PD

Methods

Norming studies for stimuli used in the predictive visual world paradigm task = It is difficult for readers to understand what the problem was and what justified the inclusion of additional stimuli. Please give an example of problematic items and replacements or move this paragraph further in the section.

Provide more information on normative scores for the telephone administrated MOCA. What is the cutoff score for normal cognition? Did all participants get a score above the cutoff?

Variability in item ratings correlate significantly with age (Pearson’s r = 0.03, p = 0.877) = The correlation is not significant

Three control participants and one PD participant scored > 1.5 but < 2 SD below normal limits on multiple tests and thus met criteria for mild cognitive impairment (Litvan et al., 2012). = Replace symbols by the words above and below, respectively. Also, the fact that those participants were not include further justifies not making strong claims about recruiting “cognitively intact” participants.

In 27.7% of predictive trials and 25.1% of non-predictive trials, participants were already fixating the target image just prior to sentence onset. Because the present study intended to examine only agent-, verb-, and target-driven increases in fixations on target objects, these target-anticipated trials were removed from the analysis. = Add a note explaining this in figure captions.

By the same token, why not eliminate sentences in which the participant was already fixating the agent distractor? No move is necessary until the verb.

Even so, by the end of the agent window, the proportion of fixations on the target interest area increased to approximately 36.1%, significantly higher than chance (χ2(1564) = 102.88, p < .0001) = By the end of the agent, two words were more likely to be fixated: the target and the agent distractor. I am not convinced that it is appropriate to run analyses that use 25% for each picture as the threshold for chance fixation at that point of the experiment.

Using the same colour coding for Figure 4 as for the other Figures is misleading because the readers needs to read the methods very carefully and look at the Appendix to realise that those words were not the same as those used in the main task.

Norming = was the agent/target relationship as strong as the agent/agent distractor relationship? Was that tested? What about the verb/target and verb/verb distractor relationship?

Rating of high vs. low motion verbs seems is based on a very small number of participants. This should be acknowledged as a limitation.

Conclusion

Thus, the fact that all of the sentences that participants heard in the present study were

semantically plausible is a strength of the study. = Some of the sentences included words that fit better in a non-count use (e.g., The shopper saves money vs. The shopper saves the money).

In addition, many of the distractor objects in the current study fit the sentences reasonably well, albeit at a lower probability than the target object. = The assumption that “chance” fixation is 25% at all points is not met. Analyses should not rely on chance level, or chance level should be specified clearly.

One limitation of the present study is that we did not carefully control the action content

of the verbs used in the predictive sentences. = This is an important limitation. There are other limitations related with words, such as the use of verbs that are homonyms with nouns (e.g., rocks), lack of control for frequency, and the use of written words in norming tasks vs. pictures in experiments. Pictures were not necessarily the most prototypical representations of the concept, and some pictures illustrated scenes/persons instead of simple objects (e.g., jungle, fugitive, courtroom).

Reviewer #2: A visual world study investigated predictive sentence processing in Parkinson’s disease. Participants heard sentences like “The fisherman rocks…” while viewing visual arrays with targets like a boat. In contrast to the hypotheses, predictive fixations to targets did not differ between participants with PD and controls.

This research has many strengths. Prediction has important theoretical implications and is of clear interest in the sentence processing literature. This study addresses novel and interesting questions about prediction in PD, which are likely to make an important addition to the literature. In addition, the introduction is clear and synthesises the two literatures well, and the method makes effective use of norming and controls. Before I am able to recommend publication, I encourage addressing the following weaknesses.

PREDICTION

The analyses do not compellingly address a fundamental issue: were participants predicting? The analyses establish that fixations to targets increased over time when participants heard predictive sentences (e.g., including prior to target word onset). However, a not dissimilar pattern was also observed in baseline (i.e., nonpredictive) sentences (e.g., see Figure 4, in which fixations to targets also increased prior to target word onset). It's also not clear how the targets compared to the various nontargets. Thus, I encourage reporting analyses that explicitly address whether the predictable targets were fixated significantly more than the nonpredictable nontargets, as is typical in the literature.

TARGET-ANTICIPATED TRIALS

Relatedly, I'm concerned that eliminating target-anticipated trials may create more problems than it solves. Among them:

(1) It makes it problematic to compare predictable targets and nonpredictable nontargets (and by extension, to address whether participants were predicting).

(2) It makes it problematic to compare targets and nontargets prior to sentence onset (and by extension, to asses potential extraneous biases).

(3) Among non-target-anticipated trials, participants may be more likely to fixate targets later in the trial because they weren’t exploring these visual stimuli earlier in the trial.

(4) Only 27% of sentences involved high motion; eliminating a further 25% likely adds further noise.

Thus, I encourage an alternative approach.

HIGH MOTION

Relatedly, I'm concerned that the high motion analysis may simply be too noisy to yield clear conclusions. The bottom-left plot of Figure 3 (i.e., controls + high motion) suggests that the verb-related and unrelated distractors diverged BEFORE verb onset (i.e., before they had relevant information), which is perhaps best explained by noise.

BATTERY

Participants with PD did not differ from controls on any of the measures in the neuropsychological battery (Table 1). Against this backdrop, the observed (i.e., visual world) similarities may be less surprising (i.e., to the extent that the visual world reflects another cognitive task). I wonder if this pattern is typical in the PD literature? In addition, it may be worthwhile to address prior individual differences research. For example, individual differences in memory, speed of processing, etc. have been linked to predictive sentence processing; if participants with PD did not differ from controls on these measures, then they might not be expected to differ in prediction:

Huettig, F., & Janse, E. (2016). Individual differences in working memory and processing speed predict anticipatory spoken language processing in the visual world. Language, Cognition and Neuroscience, 31(1), 80-93.

Kukona, A., Braze, D., Johns, C. L., Mencl, W. E., Van Dyke, J. A., Magnuson, J. S., ... & Tabor, W. (2016). The real-time prediction and inhibition of linguistic outcomes: Effects of language and literacy skill. Acta Psychologica, 171, 72-84.

METHOD AND ANALYSES

Finally, I encourage clarifying a handful of issues:

p12 – “Norming Study 1… revealed at least one problematic component in each of the original proposed stimuli sets...”; it’s not clear why some of these materials were used if problematic.

p17 – “These analyses were conducted using the cor.test() function in R version 3.5.1”; here and throughout, the discussion can be streamlined (e.g., captured by the analysis code).

p25 – “removal also helped ensure that participants’ eye movements reflected naïve predictions based on the words in the sentences rather than predictions based on the study structure”; this raises the question, was there such structure? For example, did repeating the visual stimuli allow participants to predict targets independent of the sentences (e.g., such that once the boat was a target, it was never again a target on its subsequent presentations).

p25 – “All intermediate proportions of fixations on each interested area were rounded to either 0 (no fixation) or 1 (fixation) because the raw binned proportions essentially followed a binomial distribution”; it’s not clear why the raw eye movement data was binned if a binomial approach was to be used (i.e., prior to binning, it was presumably binomial).

p26 – “Linear term estimates indicate whether fixation proportions increase, decrease, or remain flat…”; the (i.e., logistic) analyses are modelling transformed binomial outcomes, not the curves depicted in the figures. Thus, it’s not clear if curvilinear forms are suitable.

p26 – “In each model, we additionally generated random intercepts and random linear slopes for subjects (to assess individual differences) and for items (to assess stimulus-driven variability)”; growth curve analysis is widely used to model participant fixation curves that are generated by averaging across visual world trials (i.e., yielding curvilinear forms). In contrast, it’s not clear if curvilinear forms are suitable for modelling trial-level binomial outcomes.

p28 – “by the end of the agent window, the proportion of fixations on the target interest area increased to approximately 36.1%, significantly higher than chance”; I encourage addressing important nuances within this time course. For example, was the boat fixated signifiantly more than the cradle and quilt but the same as the net?

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Reviewer #1: No

Reviewer #2: No

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PONE-D-21-22350R1Predictive language comprehension in Parkinson’s diseasePLOS ONE

Dear Dr. Roberts,

Thank you for submitting your revised manuscript to PLOS ONE. Both reviewers commend your response to their comments on your original submission. Reviewer 1 had no additional comments and Reviewer 2 had just a few minor suggestions for clarification and consistency. Therefore, we invite you to submit a revised version of the manuscript that addresses these points.

Please submit your revised manuscript by Dec 24 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

• A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
• A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

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We look forward to receiving your revised manuscript.

Kind regards,

Daniel Mirman

Academic Editor

PLOS ONE

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Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: All my comments have been addressed.

The system will not let me bypass the minimum character count, so I will add that I appreciate the efforts put into running additional analyses and integrating the comments in the revised version. The paper raises more questions than it answers, but suggestions for future studies are relevant and intriguing.

Reviewer #2: I thank the authors for their responses to my comments. The manuscript is strengthened throughout; this is particularly true of the results. I had just a few remaining minor suggestions:

1. The discussion is now clearer about the limitations of the motion results (e.g., “we interpret these results cautiously”; p39ln819). However, this isn’t reflected in the abstract, where these results receive considerable attention. Rather, I encourage acknowledging these limitations and/or limiting the discussion of these results in the abstract. Adding to this discussion (e.g., “it is unclear why a significant motion content x group interaction occurred before the onset of the verb”; p39ln821), I also encourage being explicit that these results are problematic because they imply that participants were sensitive to the content of the verbs before they’d heard them. (As a very minor comment, I think only one sentence type is described in the abstract before, “in either sentence type”; p2ln45.)

2. The verb-related distractor analyses are difficult to interpret without a baseline comparison. Paralleling the target vs. agent-related distractor t-test (p32ln710), I encourage including an analysis like a verb-related distractor vs. unrelated t-test. I also encourage reporting relevant descriptive statistics (M/SD). (As a very minor comment, I wonder if the Baseline analyses shouldn’t be presented before the Predictive analyses; as is, they almost seem unnecessary.)

3. Finally, I also encourage using graphs to capture the growth curve results in a clearer and more compelling way. For example, graphs depicting the measure under analysis (i.e., “our models predict the odds ratio of fixations on the target versus fixations on all other distractors. This odds ratio is log-transformed into “logits” of fixations on each interest area”; p28ln628) would be informative. Likewise, graphs depicting the growth curve fits would also be informative. Rather, it’s not clear how the intercept, linear, etc. growth curve results (e.g., see Table 2) map onto proportions of fixations (e.g., see Figure 2). (As a minor comment, the sample size was 48 participants, which seems at odds with, “when sample sizes are sufficiently large, e.g. >200 for linear estimates and >1000 for quadratic estimates, as was the case in the present study”; p29ln648.)

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

Predictive language comprehension in Parkinson’s disease

PONE-D-21-22350R2

Dear Dr. Roberts,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. I'm sorry there were problems with the submission portal and I'm glad they were eventually resolved.

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Kind regards,

Daniel Mirman

Academic Editor

PLOS ONE