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. 2020 Jul 23;15(7):e0228903. doi: 10.1371/journal.pone.0228903

Structural differences between REM and non-REM dream reports assessed by graph analysis

Joshua M Martin 1,¤, Danyal Wainstein Andriano 2, Natalia B Mota 1, Sergio A Mota-Rolim 1, John Fontenele Araújo 3, Mark Solms 2, Sidarta Ribeiro 1,*
Editor: Stavros I Dimitriadis4
PMCID: PMC7377375  PMID: 32701992

Abstract

Dream reports collected after rapid eye movement sleep (REM) awakenings are, on average, longer, more vivid, bizarre, emotional and story-like compared to those collected after non-REM. However, a comparison of the word-to-word structural organization of dream reports is lacking, and traditional measures that distinguish REM and non-REM dreaming may be confounded by report length. This problem is amenable to the analysis of dream reports as non-semantic directed word graphs, which provide a structural assessment of oral reports, while controlling for individual differences in verbosity. Against this background, the present study had two main aims: Firstly, to investigate differences in graph structure between REM and non-REM dream reports, and secondly, to evaluate how non-semantic directed word graph analysis compares to the widely used measure of report length in dream analysis. To do this, we analyzed a set of 133 dream reports obtained from 20 participants in controlled laboratory awakenings from REM and N2 sleep. We found that: (1) graphs from REM sleep possess a larger connectedness compared to those from N2; (2) measures of graph structure can predict ratings of dream complexity, where increases in connectedness and decreases in randomness are observed in relation to increasing dream report complexity; and (3) measures of the Largest Connected Component of a graph can improve a model containing report length in predicting sleep stage and dream report complexity. These results indicate that dream reports sampled after REM awakening have on average a larger connectedness compared to those sampled after N2 (i.e. words recur with a longer range), a difference which appears to be related to underlying differences in dream complexity. Altogether, graph analysis represents a promising method for dream research, due to its automated nature and potential to complement report length in dream analysis.

Introduction

Over the course of a typical night of sleep, the body undergoes characteristic physiological changes, such as variations in brain activity, muscle tone, body shifting and ocular movements. These changes can be categorized into different sleep stages, each with their own distinctive physiological markers. They include: the state of Rapid-Eye-Movement (REM) sleep and the non-REM sleep stages (sleep onset—N1, light non-REM—N2, and deep non-REM/slow-wave sleep—N3, formerly known as S3 and S4, [1,2].

In addition to the abovementioned physiology, changes in subjective reports of dreaming are also present between the sleep stages. For example, early studies found that awakenings during REM were highly associated with reports of dreaming (~80%), compared to non-REM awakenings (~10%) [3,4]. While this initially led researchers to believe that dreaming was an exclusive property of REM sleep, later studies showed that dream reports could be reliably obtained from non-REM stages [5]. There is now a consensus that dreaming may occur throughout the night during both REM and non-REM sleep; however, disagreement persists over whether dreaming in these distinct phases can be said to be qualitatively different. This point of contention is important, since it has implications for the underlying mechanisms responsible for mental experience during sleep. If the differences are merely quantitative, they suggest that the same underlying mechanism may generate all dreaming experience, only to varying degrees (as claimed by “one-gen theorists”, e.g. [6,7]). On the other hand, if qualitative differences are found, it suggests that the processes underlying REM and non-REM dreaming may be driven by distinct mechanisms (as claimed by “two-gen theorists”, e.g. [8]). To investigate these possibilities, research over the years has evaluated dream reports collected immediately after laboratory awakenings in REM versus non-REM sleep. Traditionally, this has been done through the use of human judges who rate dreams according to a number of pre-established scales and criteria [9]. Here, we briefly outline some of this previous research.

The first distinction to be noted between REM and non-REM dreaming relates to recall rates, which led to the original controversy about ‘REM = dreaming’. An extensive review of 35 studies by Nielsen [10] demonstrated that recall rates are considerably higher in REM (81.9% ± 9.0, mean ± SD), compared to non-REM (43% ± 20.8). However, recall rates for non-REM may vary considerably depending on the sleep stage—dream recall is at its highest during N1 and its lowest during N3.

The second and perhaps most robust difference found between REM and non-REM dreams relates to differing report lengths. The most widely used measure of report length is total recall count (TRC, [6]), which broadly reflects the number of unique words present within a dream report. Studies have consistently found that REM reports are longer than non-REM reports, both when measured in terms of TRC [6,1114] and when using the raw number of words contained in the report [1517].

Thirdly, REM and non-REM dream reports tend to differ in their qualitative character. REM reports are typically rated as more intense, bizarre, perceptually vivid, emotional and kinesthetically engaging [8,11,14] than non-REM reports, which are typically more thought-like and conceptual [16,18]. Since REM reports are typically longer than their non-REM counterparts, some authors argue that qualitative measures of REM and non-REM reports can only be meaningfully compared when residual differences in report length are discounted. In this regard, several studies have found that the apparent qualitative differences tend to diminish and even disappear after statistical controls for report length are employed [6,19]. However, even after utilizing such controls, some differences persist [2022]. Furthermore, the partialling out of report length has been methodologically questioned, since it presupposes that it is the length of a report that causes dream quality and not the other way around [8,23].

A final line of evidence comes from studies comparing REM and non-REM dream reports in terms of their structure, narrative complexity and story-like organization. Nielsen and collaborators [24, 25] found that dream reports collected after REM displayed more of a story-like organization when compared to reports collected after N2. On the other hand, Cicogna et al. [26] found no difference in the narrative continuity of REM and N2 dream reports obtained from spontaneous morning awakenings; similarly, by using a subsample from this same study [26], Montangero and Cavallero [27] found no differences in a microanalysis of 14 dream reports matched for report length.

While the differences outlined above point to some between-stage differences in dreaming, another important factor to consider is the time of night in which the dream occurs. Throughout a typical night, circadian cortical activation tends to increase, which is associated with characteristic changes in dreaming. Some of these time-dependent changes appear to be common to all sleep phases. For example, both REM and non-REM dream reports become longer [13,20,28], more dreamlike [28, 29], hallucinatory [18] and bizarre [14,30]. However, some of these effects appear to be sleep stage-specific, where, for example, selective increases in emotionality are seen in REM dreaming [14] and a selective decrease in directed thought has been observed in non-REM dreaming [18]. Additionally, the narrative complexity of REM dreams has been found to increase across the night [31,32] although such changes in non-REM dreaming are yet to be investigated.

While previous studies have analyzed the narrative complexity and story-like nature of dream reports, the word-by-word structural organization of REM and non-REM dream reports is yet to be investigated and meaningfully compared. One suitable method for such an evaluation is the analysis of word graphs, defined by a given number of nodes (N = 1,2,3…) and a set of edges (E = 1,2,3…) between them (G = N, E). When the graph represents oral or written discourse, each different word is a node, and the temporal sequence between consecutive words is represented by a directed, unweighted edge. The calculation of mean graph attributes using partially-overlapping sliding windows allows for comparisons across individuals notwithstanding verbosity differences. A non-semantic word-per-node version of this approach has revealed novel behavioral markers of schizophrenia [33,34,35], such as decreased graph connectedness [34] and a more random-like word trajectory [35]. Dream reports appear to be especially revealing of underlying thought disturbances in psychosis [34], and particularly of the negative symptoms of schizophrenia [35]. Graph connectedness has also been shown to predict cognitive functioning and reading ability in typical 6–8 year-olds [36], and to distinguish between elderly patients with Alzheimer’s disease, or mild cognitive impairments, and matched controls [37].

Here we investigated the structural organization of REM and N2 dream reports by applying non-semantic word graph analysis to a previously collected sample of dream reports obtained from controlled awakenings in a sleep laboratory. The first aim was to investigate whether REM and non-REM reports are differentially structured in terms of their graph connectedness and distance from a randomly-assembled sequence of words. The second aim was to evaluate how the graph-theoretical method compares to the most widely used measure of report length (i.e. TRC) in dream analysis, and to determine whether or not they can complement one another in this regard. Specifically, we hypothesized that: (1) REM reports will be longer than non-REM reports in terms of report length; (2) REM reports will be structurally different to non-REM reports in terms of graph connectedness and their approximation to random graphs; (3) Graph structure and TRC will change as a factor of the time of night; (4) Graph structure and TRC will be able to discern which sleep stage a dream report was obtained from; and (5) Graph structure and TRC will predict differences in the external ratings of dream complexity (as measured by the Perception Interaction Rating Scale, PIRS).

Methods

The data were originally collected at the University of Cape Town for the Master’s dissertation [38] of author Danyal Wainstein Andriano (DWA). The study used a quasi-experimental repeated measures design whereby participants spent nights in a sleep laboratory to provide dream reports.

Participants

Twenty-two adults (ages 18–25; mean = 19.71 ± 1.59), all undergraduate Psychology students of the University of Cape Town, were recruited via an online questionnaire to participate in the study. Two participants were excluded due to poor sleep architecture (1) or extreme sleep inertia (1). As a result, dream reports obtained from 20 participants (14 females) were included in the data analysis. Participants were fluent English-speakers (score of 100 or more for the verbal IQ of the Wechsler Abbreviated Scale of Intelligence [39]), reported good sleeping habits (score of 5 or less on the Pittsburgh Sleep Quality Index [40]), were moderate to frequent self-reported dreamers (at least once every two weeks [41]), and had no history/presence of illicit substance-use or sleeping/psychiatric disorders.

Sleep study

The sleep study took place at a hospital sleep laboratory where participants spent 3–4 non-consecutive nights, consisting of one adaptation night, followed by 2–3 experimental nights. During the adaptation night, participants familiarized themselves with the laboratory setting, without controlled awakenings or sleep recordings. On experimental nights, sleep was monitored by polysomnography (PSG) and controlled awakenings were performed in order to obtain dream reports and related questionnaire data. Each experimental night was separated by 2–7 days. This helped minimize any sleep deprivation effects that may have resulted from the experimental awakenings. On the experimental nights, participants arrived at around 19:00 and were prepared for sleep monitoring. DWA switched off the lights at 22:00 and woke the participants at 6:00, totaling approximately 8 hours of sleep recordings per session. Participants were woken for the collection of dream reports 5–6 times over the course of the night, including the morning awakening.

Awakening protocol

Controlled awakenings were performed in REM, N2 and N3 stages according to the online presence of defining polysomnographic (PSG) characteristics for the respective stages. For REM, the controlled awakenings were conducted 5–10 minutes after detection of muscle atonia (via electromyography; EMG), “saw-tooth” waves in brain activity (via electroencephalography; EEG) and distinct jagged eye-movements (via electrooculography; EOG). For N2 awakenings, the defining criteria included the presence of sleep spindles and K-complexes (via EEG), while N3 consisted of the presence of synchronized, high-amplitude delta waves (via EEG) and diminished muscle tonus (via EMG). In the case of N2 and N3, the length of time spent in a specific sleep stage was not always the same prior to the awakening, since sequences of sleep stability/instability were difficult to predict. At least 40 minutes of uninterrupted sleep was required between awakenings, with at least 15 minutes after a period of REM.

Dream report collection

When a participant met the defining PSG criteria for the desired stage of sleep, DWA entered the room where the participant was sleeping and called out their name until they verbally indicated that they were awake. DWA then asked them to recall and report all dream contents that they could remember. The dialogue between participants and DWA was based on the protocol established by Foulkes, Spear & Symonds [42] and Antrobus et al. [30]. Following collection of the verbal dream report, participants were asked to fill out a questionnaire containing a number of Likert scales pertinent to the aims of the original dissertation. Oral dream reports were recorded using a voice recorder and later transcribed and rated by an external judge blind to the conditions of the respective awakenings.

Word graph analysis

The free software Speechgraphs was used to convert transcribed speech into directed non-semantic word graphs (available at: http://neuro.ufrn.br/softwares/speechgraphs, see Fig 1 for an illustration of the transformation). While there are a number of graph measures derived from this analysis, here we chose to evaluate graph connectedness and graph random-likeness, which have been shown to be useful predictors in charting major changes in thought organization, such as those in schizophrenia [3436]. While both of these reflect aspects of graph structure, they are methodologically distinct and thus have the potential to complement one another in evaluating different aspects of speech structure. Direct evidence for their usefulness as complementary measures can be found in Mota et al. [35], where a linear combination of both connectedness and random-likeness attributes of speech classified negative symptoms and schizophrenia-diagnosis six weeks in advance.

Fig 1. Word graph analysis applied to dream reports.

Fig 1

Dream report represented as a directed word graph. Nodes indicated in red, edges indicated as black arrows. There are two components in this graph: one with three nodes and the other with 22 nodes. LCC and LSC measures are derived from the larger component.

Measures of graph connectedness

  1. Edges (calculated by the total number of edges present in the graph).

  2. Largest Connected Component (LCC; calculated by the number of nodes in the maximal subgraph in which all pairs of nodes are reachable from one another in the undirected subgraph).

  3. Largest Strongly Connected Component (LSC; calculated by the number of nodes in the maximal subgraph in which all pairs of nodes are reachable from one another in the directed subgraph, i.e. A leads to B, B leads to A).

Sliding window to control for report length

Given that connectedness attributes are highly collinear with word count [34], and that REM reports are typically longer than those of non-REM [6], any overall connectedness differences found when using the entire reports in the transformation would be heavily confounded by differences in report length and thus would not be informative. To control for such residual effects, we employed a sliding window method, which controls for word count by dividing the report up according to the window size employed (see Fig 2, for an illustration). A moving window with a fixed length of 30 words and overlap of 29 words was used along each dream report to calculate separate graph measures for each respective window. After reaching the end of the document, the mean value for each measure was calculated across all windows comprised by each report. The window size was based on evidence that 30-word windows are more informative than comparatively smaller sized windows (10 or 20 words; see [34]).

Fig 2. Illustration of the sliding window method.

Fig 2

This example uses a window length of 15 words and an overlap of 10 words. While graphs from the first two windows are shown here, the window is applied across the entire dream report, after which an overall average is calculated.

Comparison with random graphs

To investigate the random-like connectedness of dream reports, we compared each transformed report to 1,000 random graphs, which are assembled using the same number of nodes and edges, but whose word-order is arbitrarily shuffled (Fig 3). Random z-scores for each graph were calculated through subtracting the mean (mrLCC, mrLSC) of the random graph distributions from the original LCC and LSC graph values and dividing the result by their respective standard deviations (sdrLCC, sdrLSC). Graphs that approximate random graphs are those whose z-scores approximate to 0.

Fig 3. Illustration of random shuffling.

Fig 3

Word order from the dream report is randomly shuffled 1000 times. The abbreviations “mr” and “sdr” denote the respective mean (mrLCC, mrLSC) and standard deviation (sdrLCC, sdrLSC) scores calculated from this distribution of 1000 shuffled reports. An overall measure of random-like quality is then estimated using the average scores of LCC and LSC based upon this iteration.

Total Recall Count (TRC)

TRC is an objective measure of report length, which was rated by the researcher, as well as two external judges blind to the awakening conditions. It is measured by the total number of words used to describe any mentation experienced prior to awakening, excluding repetitions, redundancies, “ums” and “ahs”, corrections and external commentary on the dream [6]. It is widely used in dream research and known to be one of the best measures to distinguish between REM and non-REM mentation [6]. The measure has been more recently revised under the new name Word Count Index [14].

Perception-Interaction Rating Scale (PIRS)

The PIRS was constructed for the purposes of the original dissertation [38]. The scale was rated by the researcher, as well as two external judges trained to score the dream reports according to an ordinal scale from 0–9, according to the level of interaction described between the dream characters and their dream environment. Low scores refer to dreams involving passive unconnected thoughts and imagery, while high scores correspond to dreams involving active engagement with one’s environment and include interconnected scenes characteristic of an ongoing narrative (see S1 Text for an overview of the different levels). The scale was developed as a measure of overall dream quality and quantity, and therefore as a proxy of the overall complexity of the dream report.

It is important to distinguish the term “Dream Report Complexity” as it is used here from the term “Network Complexity”, which can be used to describe the presence and extent of non-trivial characteristics present in a given graph/network. While both of these terms share the label of “complexity”, they describe very different aspects of the dream report that may bear no relation to one another (e.g. a complex dream experience may be verbally reported in such a way that it results in a relatively simple network). To avoid ambiguities, where the term “Dream Report Complexity” is used, we wish to refer to the complexity of the mentation described by the dreamer, as is operationalised by the PIRS. Thus, for the purposes of this article, “dream report complexity” can be considered synonymous with “ratings in PIRS”.

Ethics and informed consent

The study was approved by the Psychology Department’s Ethics Committee at Cape Town University prior to data collection. All participants were fully informed about the study, signed consent forms, and were financially compensated for their involvement with R400 (approximately $45 USD at the time of the study) for spending two experimental nights in the sleep laboratory. Participant information was kept strictly confidential. The research and compensation of participants were conducted in accordance with the established guidelines set out by the University of Cape Town’s Code for Research and the Helsinki Declaration for human experimentation.

Data analysis

We performed all analyses in the R environment [43]. Wilcoxon sign-rank tests were used to evaluate differences in REM and non-REM reports, while hierarchical model comparison was used to test the remaining hypotheses. In these cases, generalized linear-models or cumulative link models were compared using the log-likelihood ratio differences of respective models to estimate the significant contribution of individual predictor variables. Models were constructed in a bottom-up manner such that individual predictors are included whose addition significantly improves the fit of the model, following their inclusion. Where applicable, sleep stage as a fixed effect (i.e. REM or N2) is included first as we expect differences in dream reports to exist here based on previous literature. Following this, TRC and variables of graph structure are entered individually to evaluate their respective contribution as predictor variables. Where significant predictors are found, composite models are then considered to evaluate whether measures may complement one another in predicting the outcome variable. To control for the independence of observations, participant medians were used for Wilcoxon sign-rank tests, and mixed effects models were used to model random effects across participants and experimental nights. To evaluate potential confounds, two confirmatory analyses were run to evaluate the influence of the presence of common words as well as the overall number of paragraphs present in the report. A table reporting the correlations between predictors and other variables of interest can be found in the supplementary material (see S1 Table).

Results

Dream recall and report complexity

A total of 198 controlled awakenings were performed during REM and N2 sleep, resulting in the collection of 146 dream reports from 20 participants (see Fig 4 for an overview). Dream recall was more prevalent following REM awakenings (90.74% vs. 72.39), while following N2 awakenings participants were more likely to report having not dreamt (19.40% vs. 7.41%) or to have had a white dream (15.67% vs. 1.85%)—an experience where subjects feel as if they were dreaming but are unable to recall any content. For the final sample in our analysis, 13 dream reports (REM = 3; N2 = 10) were excluded, as they did not meet the minimum word count of 30 words. This resulted in a final sample of 133 reports (N2 = 87; REM = 46). The elevated proportion of N2 reports in our sample reflects the greater number of awakenings that were performed in N2, since non-REM dreaming was the main interest of the original protocol [38]. Of the 133 dream reports utilized in the final sample, those obtained from N2 awakenings more often described isolated visual imagery (42.53% vs. 15.21%) or conceptual, non-visual experiences (13.79% vs. 8.70%)., while those obtained from REM awakenings described more elaborate dream sequences indicative of an ongoing narrative (75.09% vs. 43.68%).

Fig 4. Stacked bar plot showing prevalence of dream reports and type of mentation recalled.

Fig 4

REM vs. N2 differences in graph structure and TRC

We first aimed to investigate differences between REM and non-REM reports. Wilcoxon sign-rank tests were used to compare the participant medians obtained in REM and N2 (see Table 1). We found that REM reports had significantly higher Edges, LCC, LSC and TRC scores compared to N2 reports, a difference with a moderate to large effect size. No significant differences in random-likeness were observed between REM and N2 (i.e. LCCz and LSCz).

Table 1. Results from Wilcoxon sign-rank tests (n = 40).

REM N2 Z-score effect size (r) p-value
TRC 51.50 ± 41.00 34.75 ± 13.31 -3.29 .533 .001
Edges 28.65 ± 0.63 28.37 ± 0.60 -2.13 .346 .033
LCC 23.70 ± 1.08 22.41 ± 1.15 -3.19 .517 .001
LSC 16.67 ± 2.61 16.10 ± 2.44 -1.97 .320 .048
LCCz 1.47 ± 1.00 1.36 ± 0.37 -0.68 .110 .498
LSCz 3.76 ± 0.86 3.66 ± 0.99 -0.38 .062 .701

Values that reach statistical significance (α < .05) are shown in bold.

Testing for time of night effect

We next investigated whether TRC and graph measures (Edges, LCC, LSC, LCCz, LSCz) could predict the time of night in which dream reports were obtained. This corresponds to checking for a time of night effect. We first entered sleep stage as a variable for model comparison, since we were interested in whether changes across the night are observed independent of any residual differences that exist between the sleep stages. As a result, variables of interest (Edges, LCC, LSC, TRC, LCCz, LSCz) were entered individually to a model containing sleep stage, to investigate whether their addition improved the overall fit of the model. From the resultant models, none of the variables were found to significantly improve the overall fit (see Table 2). Thus, no time of night effect was found in the present data for any of the respective predictor variables.

Table 2. Results from generalised linear mixed models in predicting time of night.

Individual Predictors Pseudo R2 Pseudo R2 Change p
Sleep Stage .011 .011 .229
Sleep Stage + TRC .022 .011 .228
Sleep Stage + Edges .016 .006 .386
Sleep Stage + LCC .021 .010 .240
Sleep Stage + LSC .011 <.001 .960
Sleep Stage + LCCz .013 .002 .615
Sleep Stage + LSCz .030 .019 .107

*Pseudo R2 change values are calculated in comparison to a model containing sleep stage, while Pseudo R2 are calculated in relation to the null model. Time of night is measured according to minutes elapsed since lights off (i.e. 22:00 PM). Where applicable, Pseudo R2 change and p-values reflect the contribution of the predictor highlighted in bold.

Distinguishing sleep stage based on graph structure and TRC

Testing individual measures

To test how graph structure compares to TRC as a means to discern sleep stage, we constructed generalised linear models with a binomial (REM/N2) outcome, to examine whether aspects of graph structure could significantly distinguish between reports obtained from REM and N2 sleep and how they may relate to the widely used measure of TRC in this regard. The analysis found that the addition of LCC and TRC significantly improved a null model in predicting differences in REM and N2 (Table 3). The differences after adding Edges, LSC, LCCz, and LSCz were not found to be significant. Thus, mirroring the differences found in our Wilcoxon-sign rank tests, we found that TRC and LCC were the best performing variables in detecting differences amongst REM and N2 reports; however, unlike before, Edges and LSC were not found to be significant predictors in this regard.

Table 3. Results from generalised linear mixed models in predicting sleep stage.
Individual Predictors Pseudo R2 Pseudo R2 Change p
TRC .095 .095 .002
Edges .011 .011 .307
LCC .069 .069 .009
LSC .002 .002 .676
LCCz <.001 <.001 .804
LSCz .011 .011 .313
Composite Models Pseudo R2 Pseudo R2 Change p
TRC + LCC .138 .048 .033
LCC + TRC .138 .074 .007

Values that reach statistical significance (α < .05) are shown in red. Significance testing and Pseudo R2 are calculated in comparison to the Null Model for the first set of individual measures, and calculated in comparison to a model containing either TRC or LCC in the composite analyses. Where applicable, Pseudo R2 Change and p-values reflect the contribution of the predictor highlighted in bold.

Testing for complementary measures

We next investigated whether LCC and TRC could act as complementary measures to one another in the discernment of sleep stage. In this regard, we tested whether the addition of LCC to a model containing TRC would significantly improve the fit of the model in predicting differences in sleep stage. The model containing both TRC and LCC was found to be significantly better at predicting sleep stage than TRC alone (Table 3). We performed the same analysis, this time seeing whether TRC could add significantly to a model containing LCC. Once again, the difference between the models was significant, indicating that TRC and LCC are complementary measures in discerning sleep stage.

Testing the relationship to dream report complexity

Testing individual variables

We next evaluated whether TRC and measures of graph structure are related to external ratings of dream complexity (i.e. PIRS). The null model adopted for comparison contained the fixed effect of sleep stage, since we are interested in whether the explanatory variables can significantly improve the fit of the model over and above differences in complexity between the sleep phases.

Table 4 shows that the addition of Edges, LCC, TRC and LCCz to a model containing sleep stage significantly improved the fit of the model in predicting PIRS scores for these variables, while LSC showed a significant trend in the same direction. LSCz was not found to be statistically significant. In terms of the direction of this relationship, the results indicated that report length and graph connectedness increases while graph random-likeness decreases in relation to increased ratings of dream report complexity. The effect sizes of graph structure measures, as estimated by a change in Nagelkerke’s pseudo-R2, were found to be of a small to medium size; the effect size for the addition of TRC was large. In order to test whether the slope of effect in predicting dream report complexity was different in REM or N2, we tested for the presence of an interaction effect between sleep stage and the fixed effects in the respective models (TRC, Edges, LCC, LSC, LCCz, LSCz). The addition of the interaction effect significantly improved the fit for only Edges (Pseudo R2 Change = .036, p = .029), but not for any of the other measures (TRC: Pseudo R2 Change = .016, p = .161; LCC: Pseudo R2 Change = <.001, p = .803; LSC: Pseudo R2 Change = .005, p = .437; LCCz: Pseudo R2 Change = .004, p = .463; LSCz: Pseudo R2 Change = .015, p = .162). We may therefore assume that, except in the case of Edges, the trends for REM and N2 groups were not significantly different from one another in their prediction of dream report complexity.

Table 4. Results from cumulative link models in predicting PIRS ratings.
Individual Predictors Pseudo R2 Pseudo R2 Change p
Sleep Stage .138 .138 <.001
Sleep Stage + TRC .588 .522 <.001
Sleep Stage + Edges .194 .065 .003
Sleep Stage + LCC .228 .105 <.001
Sleep Stage + LSC .179 .048 .012
Sleep Stage + LCCz .138 <.001 .858
Sleep Stage + LSCz .171 .038 .025
Composite Models Pseudo R2 Pseudo R2 Change p
Sleep Stage + TRC + Edges .590 .005 .430
Sleep Stage + TRC + LCC .620 .079 .001
Sleep Stage + TRC + LSC .591 .007 .336
Sleep Stage + TRC + LSCz .620 .078 .002
Sleep Stage + TRC + LSCz + LCC .629 .023 .090
Sleep Stage + TRC + LCC + LSCz .629 .023 .094

Values that reach statistical significance (α < .05) are highlighted in red. Values of Pseudo R2 Change are calculated in comparison to the sleep stage model for individual measures and in comparison to the model containing TRC and sleep stage for the composite ones. Where applicable, Pseudo R2 Change and p-values reflect the contribution of the predictor highlighted in bold.

Testing complementary measures

Given the significant relationships found, we next sought to investigate whether attributes of graph structure that were previously found to be significant could act as complementary measures to TRC in explaining dream complexity. To do so, we compared the log-likelihood ratios of a model containing TRC and the individual connectedness measures to a model only containing TRC. We found that the addition of LCC and LSCz significantly improved the fit of the model; no such effect was found for Edges or LSC. As a result, this suggests LCC and LSCz can act as a complementary measure to TRC in explaining differences in dream report complexity. We then took a final step to evaluate whether LCC and LSCz entered together could further improve the fit of these composite models. Neither model comparison was found to significantly improve the overall fit, although both showed a trend towards significance (0.05 < p < 0.10).

Dependence on PIRS in predicting sleep stage

Given that our results indicate that LCC and TRC can predict differences in sleep stage (REM vs. N2), and that both are related to measures of dream report complexity, we added a supplementary hypothesis that sought to investigate whether the ability of LCC and TRC to discern between REM and N2 reports is independent of differences in PIRS ratings. By comparing the log-likelihood ratios of the respective models, we found that the addition of either LCC (Pseudo R2 Change = .018, p = .197), TRC (Pseudo R2 Change = < .001, p = .928) or both LCC and TRC (Pseudo R2 Change = .019, p = .432) did not significantly improve the fit of a model containing the predictor of PIRS in sleep stage discernment. This suggests that once differences in dream report complexity are partialled out, both TRC and LCC are unable to statistically distinguish between REM and N2 dream reports.

Follow-up analyses: Controlling for common words and number of paragraphs

Following our main analysis we performed two follow-up analyses to evaluate the effects of two potential confounds to our results. Firstly, given that graph loops are often intersected by common pronouns, prepositions and conjunctions, we sought to investigate whether the above results can be explained merely by the increased occurrence of these classes of words in certain dream reports. To do this, we applied a standard list of English NLTK stop-words (accessed via https://gist.github.com/sebleier/554280) to the dream reports and re-evaluated the analyses where graph attributes were found to be significant predictors (see S1 Appendix). We were able to reproduce our findings above with comparable results: despite a reduced sample size (n = 113), all findings were either still found to be significant, or still demonstrated a trend towards significance in the same direction. Effect sizes were comparable to before, and in some cases were found to be even stronger (e.g. in predicting dream report complexity).

Secondly, given that LCC and Edges scores are affected by distinct graph components, we next sought to rule out the possibility that our findings may merely be reflected by differences in the overall number of paragraphs, deriving from different turn-taking between the participant and researcher. Indeed, when comparing the average number of paragraphs we found that, on average, N2 reports had on average more paragraphs (median = 3.5, standard deviation = 1.75) than REM ones (median = 2.5, standard deviation = 2.09). This raises the possibility that differences in graph structure may merely reflect an increased occurrence in the number of paragraphs in N2 dream reports. To control for this confounding influence, we performed a supplementary analysis partialling out the number of paragraphs before evaluating the ability of graph measures to predict differences in sleep stage and dream report complexity (see S2 Appendix). Once again we were able to reproduce our main results: the addition of graph structure predictors was still found to improve the overall fit of the respective models. There were two exceptions: LCC failed to complement TRC in predicting sleep stage, and LSCz failed to predict differences in dream report complexity. Nonetheless, both of these cases demonstrated a significant trend in the same direction (LCC, p = .062; LSCz, p = .061). Effect sizes were slightly reduced, which is not surprising given that any shared explanatory variance between graph structure measures and the number of paragraphs would have been partialled out by the control analysis. Overall, given that our core findings were replicated, we interpret this to rule out common words or differences in paragraphs as potential confounds to the present results.

Discussion

Here we investigated differences in the structural organization of REM and non-REM dream reports, and how structural non-semantic graph measures may compare to report length (i.e. TRC) in dream report analysis. This is the first study to demonstrate that when represented as graphs, REM dream reports possess a larger structural connectedness compared to N2 reports, a result that cannot be explained by differences in report length. It also indicates that graph structure, both in terms of connectedness and its random-likeness, is informative of dream report complexity, where more complex dreams are associated with larger connectedness and less random-like graph structures. Finally, the results demonstrate that aspects of graph connectedness (specifically LCC and LSCz) can act as a complementary measure to TRC in predicting differences in REM and non-REM dream reports and overall ratings of dream complexity. Collectively, our results complement the existing literature reporting qualitative differences in REM and non-REM dream reports, and point to non-semantic graph analysis as a promising automated measure for future use in dream research.

REM reports are longer and have larger connectedness compared to N2

The results of the present study are consistent with findings in previous studies pointing to overall differences in REM and non-REM dream reports. Firstly, we found that dream recall is higher in REM than N2 awakenings [10]. Secondly, we found that qualitatively, REM dreams were more part of an ongoing narrative while non-REM dreams involved non-visual, conceptual recall. This is consistent with previous studies showing that REM dreams are more hallucinatory [18] and story-like [25] while non-REM dreams are often thought-like [18] and conceptual [16]. Finally, in our sample, REM reports were typically longer than N2 ones (i.e. higher TRC), supporting previous studies showing that one of the most robust differences between these two groups relates to report length [6].

Through using a sliding window method, to control for differences in report length, we aimed to investigate whether intrinsic structural differences are found between these reports from REM and N2. The results showed that REM reports had larger connectedness compared to N2 in terms of LCC, Edges and LSC with moderate to large effect sizes. On the other hand, when comparing dream reports to those that were randomly shuffled 1,000 times, we did not find any differences in REM and non-REM reports in their random-likeness. This suggests that, on average, words contained in REM reports tend to recur with a longer range compared to those in N2 reports, forming longer loops and far-reaching connections, resulting in larger connectedness. However, they suggest that these structural differences are not accompanied by differences in the way that they approximate to random speech, such as is found in people suffering from schizophrenia [35]. In terms of a time of night effect, we were not able to replicate findings from previous studies [14,30], which demonstrated changes in qualitative and quantitative aspects of dream reports across the night. In our study, both graph measures and TRC did not change as a factor of the time of night. Given that TRC has been found to change significantly across the night [11,13], it is unclear whether the findings for graph structure here reflect a genuine null effect or a particular characteristic of our sample. Given that controlled awakenings were also conducted during N3 in our sample, we speculate that sleep deprivation from numerous awakenings may have displaced sleep architecture, resulting in changes to the characteristic sleep cycle needed for a time of night effect to occur.

These results collectively suggest that dream reports are less frequent in N2, and when they are present, they are typically shorter, more thought-like and have smaller connectedness compared to their REM report counterparts. Given that many differences in REM and non-REM reports are highly diminished or even disappear after controlling for length [6], these findings also have value in supplementing the small group of studies that have found differences between these sleep stages over and above residual differences in report length [2022]. Further research may investigate the time of night effect, in order to clarify whether graph connectedness increases across the night in a similar fashion to other dreaming variables reported in previous studies [14,30].

Graph connectedness in relation to dream reports across the sleep cycle

Previous studies have found that graph measures from dream reports can be particularly informative of the thought disturbances that underlie psychosis [33,35]. Such findings naturally prompt comparisons to the long-held phenomenological comparisons [44,45] of dreaming as a model for psychosis [34,46]. One of the hallmark differences between REM and non-REM dreaming is the more bizarre, hallucinatory nature of the former [18]. By extension, one may speculate that graphs obtained from REM reports would be more closely related to those of people with schizophrenia (i.e. would be less connected). However, such an interpretation is contradicted by the present findings, where REM graphs had on average larger connectedness compared to N2 graphs, and not the other way round. If we were to apply this framework to our sample, it would suggest that N2 dream reports mimic the reports of those with psychosis more than REM reports do, which seems improbable according to its phenomenology. Thus, while the phenomenological aspects of dreaming may approximate the experiences of people with psychosis, the differences in the connectedness of dream reports across the sleep cycle in healthy young adults do not reflect this.

We believe a more suitable approach to the present data would be to interpret the observed differences in graph connectedness in terms of variations in the cognitive ability of participants to retrieve and organize their dream experiences. This is in accordance with findings that graph connectedness tends to increase in healthy cognitive development in children [36] and declines in age-related dementias [37] and some psychopathologies [3335] where cognitive impairment is commonly observed.

For the present study, we postulate that the observed changes of graph connectedness in dream reports across the sleep cycle may be conceivably affected by two main factors. The first factor is related to sleep inertia and the immediate effects upon cognition of the sleep/wake transition, whereby memory and attention processes may be impaired. Since sleep inertia is more marked in N2 compared to REM [47], one can imagine that this may exert a more negative impact on the ability to mentally organise one’s thoughts in N2, leading to the decrease in report connectedness as compared to REM.

The second factor is related to the nature of the dream experience itself. Since the quality of dreaming may vary considerably, both within and between sleep states, it is possible that the ability to organize experience into a verbal report may be influenced by the underlying complexity of the dream experience to be described. In this sense, dream experiences that are coherent, immersive and story-like may be more easily organized into a report with larger connectedness, while dream experiences that are fragmented and isolated are relatively more difficult to organize mentally and thus are structurally less connected. While complex dream narratives may occur in N2, REM physiology may provide more favourable conditions for such dreams to occur, given the diffuse cortical activity and increased activation of the motor cortex [48] coupled with muscle atonia, allowing for an immersive, interactive narrative to develop uninterrupted.

To estimate the relative contribution of these two processes, three findings are of potential interest. Firstly, once we partialled out differences in PIRS ratings, we found that LCC could no longer distinguish between REM and N2 dream reports. Secondly, by using a model containing sleep stage as a statistical comparison, we showed that graph connectedness could significantly predict PIRS over and above any differences in sleep stage (i.e. when graph differences related to the sleep stage are partialled out). Finally, with the exception of Edges, no significant interaction effect was found between the graph attributes and sleep stage as a variable, indicating that the modeled relationship between TRC and graph connectedness with PIRS was largely comparable for both REM and N2 dream reports.

On the surface these results appear to argue against the role of sleep inertia, since graph connectedness is more closely related to differences in ratings of dream complexity than it is to differences between the REM and N2 sleep stages. However, the PIRS ratings themselves may be confounded by sleep inertia, since they too are based upon verbal reports collected after awakening. Given this possibility, the role of sleep inertia cannot be ruled out as an explanation for the present findings. To tease apart the relative contribution of these two processes, future research should investigate the relationship between the narrative/story-like complexity of dreams and their graph connectedness in different samples. Since the narrative complexity of dream reports persists even after a period of time has elapsed [31], one may uncouple the effects of sleep inertia from dream complexity through analysing and comparing the story-likeness and structural connectedness of reports obtained immediately after awakenings to another set of reports that describe the same dream experiences during the night, after a delay, where any residual cognitive effects of the sleep/wake transition should be greatly diminished. Clearly, since the two explanations are not mutually exclusive, graph connectedness is likely to be affected by a combination of these factors, as well as other factors not considered here.

Graph analysis as a method for dream research with clinical potential

By utilizing hierarchical model construction in discerning sleep stage (REM vs. N2) and levels of dream complexity (as measured by the PIRS), we were able to probe how graph connectedness compared to TRC in modeling these variables of interest and whether it could act as a complementary measure in this regard. We found LCC could predict differences in sleep stage and could significantly improve a model containing TRC in this prediction, albeit with a small effect size. We also found that individually LCC and LSCz could significantly improve a model containing TRC in predicting ratings on the PIRS. Given that TRC is one the most widely used measures to distinguish REM and non-REM reports, this finding is of particular important since it suggests that graph-based analyses of report structure may act as a complementary measure to TRC in discerning the sleep stage of a report and measuring underlying aspects of dream complexity. While Edges and LSC did not significantly discern REM and non-REM dreams or significantly improve models containing TRC, they still showed promise in predicting differences in dream report complexity.

As a whole, these findings point to non-semantic graph analysis as a potentially valuable tool for dream report analysis. The automated nature of this analysis means that it is fast, low-cost and avoids the biases and problems of reliability inherent in methods that involve human rating systems [9]. It offers a number of methodological advantages, as it may be applied to large corpora of dream reports that may otherwise be too time-consuming and/or expensive to apply traditional, human-based rating systems. The advent of the Dream Bank [49], which now holds more than 20,000 dream reports represents an example where computational methods such as non-semantic graph analysis may hold particular value.

The present study also extends and corroborates previous findings on the non-semantic graph structure of dream reports in healthy controls, which differs substantially from the structures observed in dream reports from patients with schizophrenia or Alzheimer’s disease [3337]. Exploration of the clinical implications of the method must include the assessment of patients with various non-REM or REM sleep disorders, as well as a fine-grained comparison of the effects of psychiatric medications on the structure of dream reports.

Limitations and future perspectives

In light of the present findings, a number of limitations need to be considered. Firstly, it is unclear how sleep inertia may have affected the graph connectedness results. While we have shown statistically that such an influence is unlikely to fully explain differences in graph connectedness, it cannot be ruled out. Secondly, our participant median TRC estimates in REM (51.5) and N2 (34.75) are closer to one another compared to those cited in previous studies (e.g. [11] REM—40, N2–13; [12] REM—148, N2–21). Thus, it is possible that TRC’s potential as a measure to predict differences in sleep stage may be diminished here, due to inherent characteristics of the sample. Finally, while we have reported differences in REM and non-REM reports, the scope of our non-REM findings is restricted to N2 reports. Future studies incorporating N1 and N3 reports, as well as waking mentation reports, should enhance our understanding of these changes across the sleep/wake cycle in relation to underlying mentation.

Conclusions

We have shown that the word-to-word structural organization of dream reports is informative about the sleep stage in which it was obtained and the overall complexity of the dream report, even when differences in report length are partialled out. Our results are consistent with previous findings showing that dreaming in N2 as compared to REM is less frequently recalled and, when present, is shorter, less intense and more thought-like and conceptual. Our results also supplement previous research by showing that N2 reports display smaller connectedness (i.e. words recur over a shorter range) compared to their REM report counterparts. Although a time of night effect has been found in previous literature, we were not able to replicate the finding here, possibly due to the displacement of deep sleep due to multiple experimental awakenings in N3. While the effects of sleep inertia cannot be ruled out, the observed differences in graph structure appear to reflect underlying differences in the dream complexity, where coherent, story-like dream experiences (more commonly found in REM), are more likely to be organized with larger connectedness and less random-like report structure. These findings represent a significant step towards characterizing the evolution of the structure of mentation across the various phases of the sleep cycle. They also point to non-semantic graph analysis as a promising automated measure for sleep research due to its sensitivity to dream complexity and its ability to complement report length in the analysis of REM and non-REM dream reports. Further research can replicate and extend these findings through clarifying the effects of sleep inertia on graph connectedness and evaluating the evolution of graph structure according to the time of night effect. Such investigations can enhance our knowledge of dreaming and its various manifestations throughout the night, while providing additional evidence for the application of automated graph-based methods in dream research.

Supporting information

S1 Text. Overview of levels of Perceptual Interaction Rating Scale (PIRS).

(DOCX)

S1 Table. Correlation matrix showing relationship between variables of interest.

(DOCX)

S1 Appendix. Showing results for follow-up analysis controlling for the occurrence of common words (via NLTK list).

(DOCX)

S2 Appendix. Showing results from follow-up analysis partialling out number of paragraphs.

(DOCX)

Acknowledgments

We would like to thank Mariza van Wyk and Michelle Henry for their help in evaluating the dream reports as external judges and Gal Adar and Tony Friend for the motivational support in the writing of the manuscript.

Data Availability

All relevant data are within the manuscript and its Supporting Information files.

Funding Statement

Authors from Brazil received funding from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; www.capes.gov.br), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; www.cnpq.br), Financiadora de Estudos e Projetos do Ministério da Ciência e Tecnologia (FINEP; www.finep.gov.br), and Fundação de Apoio à Pesquisa do Estado do Rio Grande do Norte (FAPERN; http://www.fapern.rn.gov.br/). SR was supported by CNPq grants 308775/2015-5 and 408145/2016-1, CAPES-SticAMSud, and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; www.fapesp.br) grant #2013/07699-0 Center for Neuromathematics. Authors from South Africa received funding from the University of Cape Town (www.uct.ac.za) through fund # 457091 to MS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

Stavros I Dimitriadis

18 Mar 2020

PONE-D-20-01935

Structural differences between REM and non-REM dream reports assessed by graph analysis

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The reviewer raised issues about the description and also the choice of the methodology proposed by the authors.

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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: Yes

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

Reviewer #1: Yes

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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: Yes

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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

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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: In this paper, the authors use non-semantic graph analysis to analyze the structure of REM and non-REM dream reports. They extract measures of graph connectedness from these dream reports to determine whether REM and non-REM dream reports differ in terms of their structures, whether these measures outperform the traditional measure of total recall count (TRC), whether these measures and TRC can complement each other in predicting sleep stage, and whether any of the measures relate to a measure of dream complexity. The authors conclude that certain graph measures can complement the use of TRC in predicting sleep stages, and since this graph analysis is simple and automatic, it could be useful in future studies.

While this paper is well motivated and suggests a potentially useful method, we have concerns mostly regarding aspects of the graph analysis and how these results are interpreted. Major and minor comments outlined below.

Major comments:

1. We are concerned about the theoretical interest of LCC/LSC. Inspection of Fig1 suggests that these measures are largely determined by the presence of common conjunctions, prepositions, and pronouns (e.g., “and”, “of”, “I”). Is it true that most of the intersection points are on these words? If so, the results could simply indicate that people use more conjunctions after REM awakenings.

This relates to the possibility mentioned in the discussion (p. 27) that the differential relationships between graph connectedness and PIRs in REM and non-REM dream reports could potentially be explained by increased sleep inertia after non-REM sleep, or differences in how the dream is reconstructed in language due to differences of cognitive state. The authors argue against this because controlling for PIRS eliminates the ability of TRC or LCC to predict sleep stage, but since PIRS data is also collected after awakenings it could similarly be affected by the (in)ability to construct a dream narrative.

2. TRC is framed as contrasting with graph-based measures, but total recall count (TRC) should be highly correlated with the total number of nodes in a full dream graph. Correlations between these measures and between all measures of interest should be reported.

3. The selection of the chosen graph measures should be more strongly justified—for example, in Mota et al. (2014) [ref. 34], graph connectedness was also assessed with average shortest path, average degree, and average clustering coefficient. These measures average across nodes in a graph, therefore adjusting for graph size. Use of these measures might obviate the need to use sliding 30-word windows, which restrict the analysis to the structure of subgraphs and can’t capture the global graph structure; this approach also likely underweights the structures at the beginning and end of the dream report, which could be informative.

4. For the LCC/LSC analysis, if the graphs are derived from temporal word relationships in dream reports, why would the graph be split into different components (e.g., a large component and small component, Fig1A)? Presumably every word is either preceded or followed by another, so this isn’t clear. Is there a pause length that was used to separate the components?

5. We are confused as to the purpose of the “random-likeness” measure. It appears to be a permutation analysis in which the authors generate a null distribution of LCC/LSC measures and compare the actual LCC/LSC measures to this null distribution, which could be used to determine whether the graph connectedness is larger than that expected by chance. Calling this a “random-likeness” measure rather than a permutation test is confusing. Since the authors subtract the mean of the null distribution from the actual values, this implies they are trying to standardize their measures in some way. If this is the case, then why not use these standardized measures throughout the whole experiment, in place of the original LCC/LSC measures?

Minor comments:

1. The authors make clear that they are using non-semantic graphs to analyze the dream reports, but do not explain why semantic graph analysis isn’t used. The highlighted distinction between narrative and conceptual content in REM and non-REM dreams, especially the descriptors “vivid, bizarre, and emotional” in the intro, suggests that interesting semantic differences might be found. Additional justification of the non-semantic approach would be useful.

2. The authors define LCC as “the number of nodes in the maximal component in which all nodes are connected to one another” (p. 11), but this is misleading as it could be interpreted to mean a fully-connected sub-graph where every node is connected to every other node. Mota et al. (2014) define it as a component in which “all pairs of nodes are reachable in an undirected subgraph” and a similar description could be used here. The definition of LSC could similarly be clarified.

3. It would be useful to disambiguate their measure of dream report complexity and network complexity, especially since network complexity likely corresponds with increased network connectedness, and the current results include a negative relationship between network connectedness and dream report complexity.

4. As it is, there are no result figures, and results are displayed in multiple tables with a large number of regression analyses, and it is hard to pull out the meaningful or important results. The descriptive statistics in Table1 could be displayed in a bar graph format.

5. In Figure 1, the font size for the word labels on the graph nodes is too small, especially in B and C.

6. The authors could consider adding a figure to help describe the methods used to create and analyze the random graphs.

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Reviewer #1: No

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PLoS One. 2020 Jul 23;15(7):e0228903. doi: 10.1371/journal.pone.0228903.r002

Author response to Decision Letter 0


3 May 2020

Major Revisions

1. We are concerned about the theoretical interest of LCC/LSC. Inspection of Fig1 suggests that these measures are largely determined by the presence of common conjunctions, prepositions, and pronouns (e.g., “and”, “of”, “I”). Is it true that most of the intersection points are on these words? If so, the results could simply indicate that people use more conjunctions after REM awakenings.

The Referee has a valid concern. In fact, conjunctions, prepositions, and pronouns tend to reduce the size of loops, and may have an indirect effect of LCC/LSC. In the revised manuscript we provide a follow-up analysis where we re-run the graph analyses using a standard list of NLTK stop-words (https://gist.github.com/sebleier/554280). For ease of interpretation for the reader and given this is to rule out a potential confound in our findings, we only re-ran the significant results from our original analysis (this also applies to the analysis pertaining to major revision 4). We were able to reproduce our findings with comparable results: despite a reduced sample size, all findings were either still found to be significant (11/13), or still demonstrated a trend towards significance in the same direction (2/13). Effect sizes were comparable, and in some cases were found to be even stronger than before (e.g. in predicting dream complexity). Given that our core findings were replicated following this control, we interpret this to rule out an increased occurrence of common words as a potential confound for the present results.

The tables reflecting the findings can be found in the supplementary material, while the code can be found in the updated R Notebook. The changes in the manuscript reflect below the main analysis and point the reader to the supplementary material for the corresponding tables.

This relates to the possibility mentioned in the discussion (p. 27) that the differential relationships between graph connectedness and PIRs in REM and non-REM dream reports could potentially be explained by increased sleep inertia after non-REM sleep, or differences in how the dream is reconstructed in language due to differences of cognitive state. The authors argue against this because controlling for PIRS eliminates the ability of TRC or LCC to predict sleep stage, but since PIRS data is also collected after awakenings it could similarly be affected by the (in)ability to construct a dream narrative.

We agree with the Reviewer’s reasoning here that PIRS may also be similarly confounded by sleep inertia and differences in post-awakening cognitive state, and thus it may not be completely ruled out. In the revised manuscript we moderate the argument and describe sleep inertia and dream report complexity as two non-mutually exclusive factors that may explain the present findings, rather than arguing for the latter. We still think it is important to show that, even though sleep inertia cannot be ruled out, the statistical relationship between graph connectedness, sleep stage and PIRS ratings is important to report on. In this regard the partialling out analyses remain useful (e.g. graph connectedness predicts PIRS beyond controlling for differences in sleep stage).

2. TRC is framed as contrasting with graph-based measures, but total recall count (TRC) should be highly correlated with the total number of nodes in a full dream graph. Correlations between these measures and between all measures of interest should be reported.

We thank the Reviewer for the useful recommendation. The revised manuscript includes a table in the supplementary material, including correlations between graph measures (original graph, sliding window and random graph), TRC, as well as simple quantitative report features of interest, such as word count and number of pauses. As the reviewer correctly points out, TRC is highly correlated with attributes in the full dream graph (Spearman’s rho, Edges = .681, LCC = .729 and LSC = .729), which drops substantially once the sliding window method is utilized (Spearman’s rho, Edges = .389, LCC = .257 and LSC = .224). We hope the added table provides sufficient information for this requirement.

3. The selection of the chosen graph measures should be more strongly justified—for example, in Mota et al. (2014) [ref. 34], graph connectedness was also assessed with average shortest path, average degree, and average clustering coefficient. These measures average across nodes in a graph, therefore adjusting for graph size. Use of these measures might obviate the need to use sliding 30-word windows, which restrict the analysis to the structure of subgraphs and can’t capture the global graph structure; this approach also likely underweights the structures at the beginning and end of the dream report, which could be informative.

We beg to differ. We chose Edges, LCC and LSC because they have been consistently the most informative measures of connectedness in previous literature [1-4]. The approach is thus simple and directed, using only measures that have been of most theoretical interest for the current study. This is also in line with more recent publications that have left out other graph measures and focused on attributes of connectedness and randomlikeness [3] . We agree that other measures may well be interesting and informative, but we feel that their inclusion may further clutter and complicate an already rather complex results section and also add further statistical controls for multiple comparisons, which could lead to an increase in Type I error. We thus wish to maintain and focus on the variables that were originally chosen.

4. For the LCC/LSC analysis, if the graphs are derived from temporal word relationships in dream reports, why would the graph be split into different components (e.g., a large component and small component, Fig1A)? Presumably every word is either preceded or followed by another, so this isn’t clear. Is there a pause length that was used to separate the components?

We thank the Reviewer for the useful recommendation. Pauses here reflect changes in dialogue between the researcher and participant. The revised methods make it clear that separate responses in the dialogue may result in different components - but not necessarily so, since the re-occurrence of a word in separate responses will link the components, as explained in Mota et. al. [5]. Please note also that while this means that pauses will be related to aspects of graph structure, the number of pauses does not directly equate to the number of nodes in LCC, since it is performed across the sliding window and not the entire graph. To rule out the possibility that our findings may merely be reflected by differences in the number of pauses, we performed a supplementary analysis partialling out the number of pauses before evaluating the ability of graph measures to predict differences in sleep stage and dream complexity (see Supplementary Analysis 2). Once again we were able to replicate our core findings: the addition of graph structure predictors was still found to improve the overall fit of the respective models. There were two exceptions to this: firstly, LCC failed to complement TRC in predicting sleep stage, while LSCz failed to predict differences in dream complexity. Nonetheless, similar to our other supplementary analysis, both of these cases demonstrated a significant trend in the same direction (LCC, p = .062; LSCz, p = .061). Thus, overall we feel that this is sufficient evidence against the interpretation that our findings can be explained by a confound deriving from differences in the number of pauses. The manuscript was revised accordingly.

5. We are confused as to the purpose of the “random-likeness” measure. It appears to be a permutation analysis in which the authors generate a null distribution of LCC/LSC measures and compare the actual LCC/LSC measures to this null distribution, which could be used to determine whether the graph connectedness is larger than that expected by chance. Calling this a “random-likeness” measure rather than a permutation test is confusing. Since the authors subtract the mean of the null distribution from the actual values, this implies they are trying to standardize their measures in some way. If this is the case, then why not use these standardized measures throughout the whole experiment, in place of the original LCC/LSC measures?

The purpose of the random-likeness measure is to provide another measure of graph structure through calculating how each graph approximates to a random like structure through comparing it to a distribution of random graphs generated through word shuffling, or permutation. It is not meant to replace graph connectedness, but rather provides an additional complementary method to evaluating graph structure which has been shown to be useful in previous applications (e.g. diagnosis of schizophrenia based on dream reports: [1-4]). Direct evidence for their usefulness as complementary measures can be found in Mota et al. [3], where a linear combination of both connectedness and random-likeness attributes of speech classified negative symptoms and schizophrenia-diagnosis six weeks in advance. Given this empirical grounding, we feel that both of their inclusion is justified in the present study. We have adjusted the methods section to make this justification explicit.

Minor comments:

1. The authors make clear that they are using non-semantic graphs to analyze the dream reports, but do not explain why semantic graph analysis isn’t used. The highlighted distinction between narrative and conceptual content in REM and non-REM dreams, especially the descriptors “vivid, bizarre, and emotional” in the intro, suggests that interesting semantic differences might be found. Additional justification of the non-semantic approach would be useful.

Perhaps the way we phrased it gave the reviewer the idea that we could either have utilised a semantic or non-semantic graph approach, and that we opted for the latter. The current approach is not related to whether a semantic or non-semantic approach is optimal for investigating dreams per se, but rather is due to the demonstrated usefulness of the current non-semantic approach to “mind-mapping” based on dream reports in cognitive development [1-4]. Semantic approaches to dreaming are indeed very interesting and have been investigated elsewhere [6]. To avoid confusion, we have changed the title from “Non-semantic word graph analysis” to “Word graph analysis” in the methods section, and adjusted the caption in Figure 1 accordingly.

2. The authors define LCC as “the number of nodes in the maximal component in which all nodes are connected to one another” (p. 11), but this is misleading as it could be interpreted to mean a fully-connected sub-graph where every node is connected to every other node. Mota et al. (2014) define it as a component in which “all pairs of nodes are reachable in an undirected subgraph” and a similar description could be used here. The definition of LSC could similarly be clarified.

We thank the Reviewer for the recommendation. The LCC and the LSC will be defined as suggested in Mota et al. [2].

3. It would be useful to disambiguate their measure of dream report complexity and network complexity, especially since network complexity likely corresponds with increased network connectedness, and the current results include a negative relationship between network connectedness and dream report complexity.

Please note that the current results indicate a positive relationship between connectedness and dream report complexity (i.e. larger LCC and LSC are related to more complex mentation). Yet, we agree with the Reviewer that dream report complexity and network complexity are measures that share the label of “complexity” but refer to distinct characteristics of the dream report that may bear no relation to one another. To avoid ambiguity, in the revised manuscript we explicitly state the difference between the two and emphasise how we wish to use the term in the article. (see below):

“The scale was developed as a measure of overall dream quality and quantity, which we infer here to represent the overall complexity of the dream report. It is important to distinguish the term “Dream Report Complexity” as it is used here from the term “Network Complexity”, which can be used to describe the presence and extent of non-trivial characteristics present in a given graph/network. While both of these terms share the label of “complexity”, they describe different aspects of the dream report that may bear no relation to one another. To avoid ambiguities, where the term “Dream Report Complexity” is used, we wish to refer to the complexity of the mentation described by the dreamer as is operationalised by the PIRS.”

4. As it is, there are no result figures, and results are displayed in multiple tables with a large number of regression analyses, and it is hard to pull out the meaningful or important results. The descriptive statistics in Table1 could be displayed in a bar graph format.

We thank the Reviewer for the valuable recommendation, which was duly followed. The tables of the revised manuscript were simplified and the different measures were sorted under sub-headings in the tables to make it easier to identify and pick out the results of interest. Table 1 and 2 was converted into a bar graph figure (Figure 4).

5. In Figure 1, the font size for the word labels on the graph nodes is too small, especially in B and C.

Point taken. The recommendation was implemented via splitting Figure 1 into three separate figures with higher resolution (Fig. 1-3).

6. The authors could consider adding a figure to help describe the methods used to create and analyze the random graphs.

We thank the Reviewer for the recommendation. In the revised manuscript, we edited and elaborated Figure 3 into a flow-chart to make it clearer how the random scores were derived.

References

1. Mota NB, Vasconcelos NA, Lemos N, Pieretti AC, Kinouchi O, Cecchi GA, Copelli M, Ribeiro S. Speech graphs provide a quantitative measure of thought disorder in psychosis. PloS one. 2012; 7(4).

2. Mota NB, Furtado R, Maia PP, Copelli M, Ribeiro S. Graph analysis of dream reports is especially informative about psychosis. Scientific reports. 2014; 15;4:3691.

3. Mota NB, Copelli M, Ribeiro S. Thought disorder measured as random speech structure classifies negative symptoms and schizophrenia diagnosis 6 months in advance. npj Schizophrenia. 2017; 13;3(1):1-0.

4. Mota NB, Sigman M, Cecchi G, Copelli M, Ribeiro S. The maturation of speech structure in psychosis is resistant to formal education. npj Schizophrenia. 2018; 4(1):1-0.

5. Mota, N. B., Weissheimer, J., Madruga, B., Adamy, N., Bunge, S. A., Copelli, M., & Ribeiro, S. (2016). A naturalistic assessment of the organization of children's memories predicts cognitive functioning and reading ability. Mind, Brain, and Education, 10(3), 184-195.

6. Altszyler E, Ribeiro S, Sigman M, Slezak DF. The interpretation of dream meaning: Resolving ambiguity using Latent Semantic Analysis in a small corpus of text. Consciousness and cognition. 2017; 56:178-87.

Attachment

Submitted filename: Rebuttal.docx

Decision Letter 1

Stavros I Dimitriadis

1 Jun 2020

PONE-D-20-01935R1

Structural differences between REM and non-REM dream reports assessed by graph analysis

PLOS ONE

Dear Dr. Ribeiro,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Reviewers raised a few more comments regarding the formatting of the draft, the consistency between main draft and supplementary material and further correction of the figures's captions.

I encouraged you to address them one by one and re-submit the revised manuscript.

Please submit your revised manuscript by Jul 16 2020 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.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

We look forward to receiving your revised manuscript.

Kind regards,

Stavros I. Dimitriadis

Academic Editor

PLOS ONE

Additional Editor Comments (if provided):

After carefully read your draft and the comments from the reviewers, I encouraged you to address them and re-submit

a new revised manuscript.

Their comments focuses on:

1) shortening of specific parts of the draft

2) improve the structure of the draft with appropriate numbering

3) align the report within the draft with the information in supplementary material.

[Note: HTML markup is below. Please do not edit.]

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: (No Response)

Reviewer #2: All comments have been addressed

**********

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

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

**********

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

**********

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: The authors have addressed the main concerns thoroughly. Appropriate control analyses have been added, and methods and measures have been clarified. Some remaining minor concerns listed below:

- It appears that “number of paragraphs” and “number of pauses” reflect the same measure, but that has not been made clear in the manuscript. For example, the follow-up analyses control for number of paragraphs, but Supplementary Table 2 includes statistics for number of pauses. The authors should make clear whether these are in fact the same measure, or if they reflect different aspects of the graphs.

- The authors ran a follow-up analysis to partial out number of paragraphs before assessing graph-based differences. To further motivate this analysis, it would be useful to include descriptive and comparison stats on number of paragraphs observed in the different sleep stages.

- Figure 2: Caption says window size is 15 words and overlap is 5 words, but the figure seems to show an overlap of 10 words.

- Figure 3: Why are some words red in the shuffled dream reports? There does not seem to be a need to highlight shuffled words, and this is confusing since nodes of graph are also red. Also, the abbreviations used in the figure (i.e., mrLCC, sdrLCC, mrLSC, sdrLSC) should be explained in the caption.

Reviewer #2: Many thanks to the authors for their detailed response and revision of the initial manuscript. All the valid points previously raised were addressed and an appropriate adjustment or rebuttal was provided. As such, I do not have any additional specific criticisms to mention. The revised version of the manuscript reads well and would be a meaningful addition to the literature of how to analyze dream reports. As an overarching impression, it could be shortened, particularly aspects such as the intro that expand to 5 whole pages and appear better suited for a master thesis than a journal paper. Each section and subsection can be numbered to facilitate reading. Finally, as this was a proof of concept study in healthy controls, it would be nice to incorporate some clinical repercussions in the end of the discussion (for example using such methods to evaluate patients with REM behavior or other sleep disorders and/or medication effects to dreams).

**********

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.

PLoS One. 2020 Jul 23;15(7):e0228903. doi: 10.1371/journal.pone.0228903.r004

Author response to Decision Letter 1


22 Jun 2020

Reviewer 1 Comments

- It appears that “number of paragraphs” and “number of pauses” reflect the same measure, but that has not been made clear in the manuscript. For example, the follow-up analyses control for number of paragraphs, but Supplementary Table 2 includes statistics for number of pauses. The authors should make clear whether these are in fact the same measure, or if they reflect different aspects of the graphs.

We thank the reviewer for pointing this out. Pauses and number of paragraphs here do refer to the same measure, although we decided to opt for the latter since it reflects turn-taking between the researcher and the participant (i.e. dreamer), as opposed to pauses in their speech per se. We have now changed the item in the supplementary table 2 to reflect “No. Paragraphs”, to make it clear that they refer to the same measure as before.

- The authors ran a follow-up analysis to partial out number of paragraphs before assessing graph-based differences. To further motivate this analysis, it would be useful to include descriptive and comparison stats on number of paragraphs observed in the different sleep stages.

We thank the reviewer for the suggestion. We now provide basic comparisons for number of paragraphs in the results section to further justify the need for this analysis.

- Figure 2: Caption says window size is 15 words and overlap is 5 words, but the figure seems to show an overlap of 10 words.

The reviewer is correct, thanks for pointing out this mistake. The figure does indeed show an overlap of 10 words, not 5. We have corrected this accordingly.

- Figure 3: Why are some words red in the shuffled dream reports? There does not seem to be a need to highlight shuffled words, and this is confusing since nodes of graph are also red. Also, the abbreviations used in the figure (i.e., mrLCC, sdrLCC, mrLSC, sdrLSC) should be explained in the caption.

We originally thought it may be useful to show which of the words had been shuffled in the resulting dream report. However, we agree with the reviewer that this is not necessary and may also be confusing due to the colouring of nodes. We have changed the highlighted text to black in figure 3 and have provided attached explanations for the abbreviations as suggested.

Reviewer 2 Comments

Reviewer #2: Many thanks to the authors for their detailed response and revision of the initial manuscript. All the valid points previously raised were addressed and an appropriate adjustment or rebuttal was provided. As such, I do not have any additional specific criticisms to mention. The revised version of the manuscript reads well and would be a meaningful addition to the literature of how to analyze dream reports. As an overarching impression, it could be shortened, particularly aspects such as the intro that expand to 5 whole pages and appear better suited for a master thesis than a journal paper. Each section and subsection can be numbered to facilitate reading. Finally, as this was a proof of concept study in healthy controls, it would be nice to incorporate some clinical repercussions in the end of the discussion (for example using such methods to evaluate patients with REM behavior or other sleep disorders and/or medication effects to dreams).

We thank the reviewer for the helpful feedback and additional suggestions. Where possible we have tried to lower the word count to make it more readable, specifically in the introduction section. We have also added a brief section at the end to reflect possible applications to psychopathology. Perhaps this is just a point of preference, but it does not seem that in general PLoS ONE articles use numbering for the sub-sections. As a result, we prefer to leave them without numbers to be standardised in terms of formatting with the other articles.

Decision Letter 2

Stavros I Dimitriadis

26 Jun 2020

Structural differences between REM and non-REM dream reports assessed by graph analysis

PONE-D-20-01935R2

Dear Dr. Ribeiro,

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.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Reading carefully the comments raised by the reviewers and your answer, I agree that your draft

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I recommend the acceptance of the manuscript.

Reviewers' comments:

Acceptance letter

Stavros I Dimitriadis

6 Jul 2020

PONE-D-20-01935R2

Structural differences between REM and non-REM dream reports assessed by graph analysis

Dear Dr. Ribeiro:

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on behalf of

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Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Text. Overview of levels of Perceptual Interaction Rating Scale (PIRS).

    (DOCX)

    S1 Table. Correlation matrix showing relationship between variables of interest.

    (DOCX)

    S1 Appendix. Showing results for follow-up analysis controlling for the occurrence of common words (via NLTK list).

    (DOCX)

    S2 Appendix. Showing results from follow-up analysis partialling out number of paragraphs.

    (DOCX)

    Attachment

    Submitted filename: Rebuttal.docx

    Data Availability Statement

    All relevant data are within the manuscript and its Supporting Information files.


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