Evidence for systematic - yet task- and motor-contingent - rhythmicity of auditory perceptual judgements
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eLife Assessment
This high-N, multi-task study offers a comprehensive examination of rhythmicity in behavioral performance during listening. It presents a valuable set of findings that reveal task- and ear-specific effects, challenging the notion of a universal rhythmicity in auditory perception. While the evidence is solid, the study would benefit from a stronger conceptual framework to contextualize and explain the observed patterns. Nonetheless, the work is likely to be of significant interest to behavioral and cognitive scientists focused on perception and neural oscillations.
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Abstract
Numerous studies advocate for a rhythmic mode of perception; however, the evidence in the context of auditory perception remains inconsistent. We propose that the divergent conclusions drawn from previous work stem from conceptual and methodological issues. These include ambiguous assumptions regarding the origin of perceptual rhythmicity, variations in listening tasks and attentional demands, differing analytical approaches, and the reliance on fixed participant samples for statistical testing. To systematically address these points, we conducted a series of experiments in which human participants performed auditory tasks involving monaural target sounds presented against binaural white noise backgrounds, while also recording eye movements. These experiments varied in whether stimuli were presented randomly or required motor initialization by the participant, the necessity of memory across trials and the manipulation of attentional demands across modalities. Our findings challenge the notion of universal rhythmicity in hearing, but support the existence of paradigm- and ear-specific fluctuations in perceptual sensitivity and response bias that emerge at multiple frequencies. Notably, the rhythmicity for sounds in the left and right ears appears to be largely independent among participants, and the strength of rhythmicity in behavioural data is linked to oculomotor activity and attentional requirements of the task. Overall, these results resolve conflicting conclusions drawn in previous work and provide specific avenues for further studies into the rhythmicity of auditory perception.
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eLife Assessment
This high-N, multi-task study offers a comprehensive examination of rhythmicity in behavioral performance during listening. It presents a valuable set of findings that reveal task- and ear-specific effects, challenging the notion of a universal rhythmicity in auditory perception. While the evidence is solid, the study would benefit from a stronger conceptual framework to contextualize and explain the observed patterns. Nonetheless, the work is likely to be of significant interest to behavioral and cognitive scientists focused on perception and neural oscillations.
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Reviewer #1 (Public review):
Summary:
This paper presents results from four independent experiments, each of which tests for rhythmicity in auditory perception. The authors report rhythmic fluctuations in discrimination performance at frequencies between 2 and 6 Hz. The exact frequency depends on the ear and experimental paradigm, although some frequencies seem to be more common than others.
Strengths:
The first sentence in the abstract describes the state of the art perfectly: "Numerous studies advocate for a rhythmic mode of perception; however, the evidence in the context of auditory perception remains inconsistent". This is precisely why the data from the present study is so valuable. This is probably the study with the highest sample size (total of > 100 in 4 experiments) in the field. The analysis is very thorough and transparent, …
Reviewer #1 (Public review):
Summary:
This paper presents results from four independent experiments, each of which tests for rhythmicity in auditory perception. The authors report rhythmic fluctuations in discrimination performance at frequencies between 2 and 6 Hz. The exact frequency depends on the ear and experimental paradigm, although some frequencies seem to be more common than others.
Strengths:
The first sentence in the abstract describes the state of the art perfectly: "Numerous studies advocate for a rhythmic mode of perception; however, the evidence in the context of auditory perception remains inconsistent". This is precisely why the data from the present study is so valuable. This is probably the study with the highest sample size (total of > 100 in 4 experiments) in the field. The analysis is very thorough and transparent, due to the comparison of several statistical approaches and simulations of their sensitivity. Each of the experiments differs from the others in a clearly defined experimental parameter, and the authors test how this impacts auditory rhythmicity, measured in pitch discrimination performance (accuracy, sensitivity, bias) of a target presented at various delays after noise onset.
Weaknesses:
(1) The authors find that the frequency of auditory perception changes between experiments. I think they could exploit differences between experiments better to interpret and understand the obtained results. These differences are very well described in the Introduction, but don't seem to be used for the interpretation of results. For instance, what does it mean if perceptual frequency changes from between- to within-trial pitch discrimination? Why did the authors choose this experimental manipulation? Based on differences between experiments, is there any systematic pattern in the results that allows conclusions about the roles of different frequencies? I think the Discussion would benefit from an extension to cover this aspect.
(2) The Results give the impression of clear-cut differences in relevant frequencies between experiments (e.g., 2 Hz in Experiment 1, 6 Hz in Exp 2, etc), but they might not be so different. For instance, a 6 Hz effect is also visible in Experiment 1, but it just does not reach conventional significance. The average across the three experiments is therefore very useful, and also seems to suggest that differences between experiments are not very pronounced (otherwise the average would not produce clear peaks in the spectrum). I suggest making this point clearer in the text.
(3) I struggle to understand the hypothesis that rhythmic sampling differs between ears. In most everyday scenarios, the same sounds arrive at both ears, and the time difference between the two is too small to play a role for the frequencies tested. If both ears operate at different frequencies, the effects of the rhythm on overall perception would then often cancel out. But if this is the case, why would the two ears have different rhythms to begin with? This could be described in more detail.
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Reviewer #2 (Public review):
Summary:
The current study aims to shed light on why previous work on perceptual rhythmicity has led to inconsistent results. They propose that the differences may stem from conceptual and methodological issues. In a series of experiments, the current study reports perceptual rhythmicity in different frequency bands that differ between different ear stimulations and behavioral measures. The study suggests challenges regarding the idea of universal perceptual rhythmicity in hearing.
Strengths:
The study aims to address differences observed in previous studies about perceptual rhythmicity. This is important and timely because the existing literature provides quite inconsistent findings. Several experiments were conducted to assess perceptual rhythmicity in hearing from different angles. The authors use …
Reviewer #2 (Public review):
Summary:
The current study aims to shed light on why previous work on perceptual rhythmicity has led to inconsistent results. They propose that the differences may stem from conceptual and methodological issues. In a series of experiments, the current study reports perceptual rhythmicity in different frequency bands that differ between different ear stimulations and behavioral measures. The study suggests challenges regarding the idea of universal perceptual rhythmicity in hearing.
Strengths:
The study aims to address differences observed in previous studies about perceptual rhythmicity. This is important and timely because the existing literature provides quite inconsistent findings. Several experiments were conducted to assess perceptual rhythmicity in hearing from different angles. The authors use sophisticated approaches to address the research questions.
Weaknesses:
(1) Conceptional concerns:
The authors place their research in the context of a rhythmic mode of perception. They also discuss continuous vs rhythmic mode processing. Their study further follows a design that seems to be based on paradigms that assume a recent phase in neural oscillations that subsequently influence perception (e.g., Fiebelkorn et al.; Landau & Fries). In my view, these are different facets in the neural oscillation research space that require a bit more nuanced separation. Continuous mode processing is associated with vigilance tasks (work by Schroeder and Lakatos; reduction of low frequency oscillations and sustained gamma activity), whereas the authors of this study seem to link it to hearing tasks specifically (e.g., line 694). Rhythmic mode processing is associated with rhythmic stimulation by which neural oscillations entrain and influence perception (also, Schroeder and Lakatos; greater low-frequency fluctuations and more rhythmic gamma activity). The current study mirrors the continuous rather than the rhythmic mode (i.e., there was no rhythmic stimulation), but even the former seems not fully fitting, because trials are 1.8 s short and do not really reflect a vigilance task. Finally, previous paradigms on phase-resetting reflect more closely the design of the current study (i.e., different times of a target stimulus relative to the reset of an oscillation). This is the work by Fiebelkorn et al., Landau & Fries, and others, which do not seem to be cited here, which I find surprising. Moreover, the authors would want to discuss the role of the background noise in resetting the phase of an oscillation, and the role of the fixation cross also possibly resetting the phase of an oscillation. Regardless, the conceptional mixture of all these facets makes interpretations really challenging. The phase-reset nature of the paradigm is not (or not well) explained, and the discussion mixes the different concepts and approaches. I recommend that the authors frame their work more clearly in the context of these different concepts (affecting large portions of the manuscript).
(2) Methodological concerns:
The authors use a relatively unorthodox approach to statistical testing. I understand that they try to capture and characterize the sensitivity of the different analysis approaches to rhythmic behavioral effects. However, it is a bit unclear what meaningful effects are in the study. For example, the bootstrapping approach that identifies the percentage of significant variations of sample selections is rather descriptive (Figures 5-7). The authors seem to suggest that 50% of the samples are meaningful (given the dashed line in the figure), even though this is rarely reached in any of the analyses. Perhaps >80% of samples should show a significant effect to be meaningful (at least to my subjective mind). To me, the low percentage rather suggests that there is not too much meaningful rhythmicity present. I suggest that the authors also present more traditional, perhaps multi-level, analyses: Calculation of spectra, binning, or single-trial analysis for each participant and condition, and the respective calculation of the surrogate data analysis, and then comparison of the surrogate data to the original data on the second (participant) level using t-tests. I also thought the statistical approach undertaken here could have been a bit more clearly/didactically described as well.
The authors used an adaptive procedure during the experimental blocks such that the stimulus intensity was adjusted throughout. In practice, this can be a disadvantage relative to keeping the intensity constant throughout, because, on average, correct trials will be associated with a higher intensity than incorrect trials, potentially making observations of perceptual rhythmicity more challenging. The authors would want to discuss this potential issue. Intensity adjustments could perhaps contribute to the observed rhythmicity effects. Perhaps the rhythmicity of the stimulus intensity could be analyzed as well. In any case, the adaptive procedure may add variance to the data.
Additional methodological concerns relate to Figure 8. Figures 8A and C seem to indicate that a baseline correction for a very short time window was calculated (I could not find anything about this in the methods section). The data seem very variable and artificially constrained in the baseline time window. It was unclear what the reader might take from Figure 8.
Motivation and discussion of eye-movement/pupillometry and motor activity: The dual task paradigm of Experiment 4 and the reasons for assessing eye metrics in the current study could have been better motivated. The experiment somehow does not fit in very well. There is recent evidence that eye movements decrease during effortful tasks (e.g., Contadini-Wright et al. 2023 J Neurosci; Herrmann & Ryan 2024 J Cog Neurosci), which appears to contradict the results presented in the current study. Moreover, by appealing to active sensing frameworks, the authors suggest that active movements can facilitate listening outcomes (line 677; they should provide a reference for this claim), but it is unclear how this would relate to eye movements. Certainly, a person may move their head closer to a sound source in the presence of competing sound to increase the signal-to-noise ratio, but this is not really the active movements that are measured here. A more detailed discussion may be important. The authors further frame the difference between Experiments 1 and 2 as being related to participants' motor activity. However, there are other factors that could explain differences between experiments. Self-paced trials give participants the opportunity to rest more (inter-trial durations were likely longer in Experiment 2), perhaps affecting attentional engagement. I think a more nuanced discussion may be warranted.
Discussion:
The main data in Figure 3 showed little rhythmicity. The authors seem to glance over this fact by simply stating that the same phase is not necessary for their statistical analysis. Previous work, however, showed rhythmicity in the across-participant average (e.g., Fiebelkorn's and similar work). Moreover, one would expect that some of the effects in the low-frequency band (e.g., 2-4 Hz) are somewhat similar across participants. Conduction delays in the auditory system are much smaller than the 0.25-0.5 s associated with 2-4 Hz. The authors would want to discuss why different participants would express so vastly different phases that the across-participant average does not show any rhythmicity, and what this would mean neurophysiologically.
An additional point that may require more nuanced discussion is related to the rhythmicity of response bias versus sensitivity. The authors could discuss what the rhythmicity of these different measures in different frequency bands means, with respect to underlying neural oscillations.
Figures:
Much of the text in the figures seems really small. Perhaps the authors would want to ensure it is readable even for those with low vision abilities. Moreover, Figure 1A is not as intuitive as it could be and may perhaps be made clearer. I also suggest the authors discuss a bit more the potential monoaural vs binaural issues, because the perceptual rhythmicity is much slower than any conduction delays in the auditory system that could lead to interference.
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Reviewer #3 (Public review):
Summary:
The finding of rhythmic activity in the brain has, for a long time, engendered the theory of rhythmic modes of perception, that humans might oscillate between improved and worse perception depending on states of our internal systems. However, experiments looking for such modes have resulted in conflicting findings, particularly in those where the stimulus itself is not rhythmic. This paper seeks to take a comprehensive look at the effect and various experimental parameters which might generate these competing findings: in particular, the presentation of the stimulus to one ear or the other, the relevance of motor involvement, attentional demands, and memory: each of which are revealed to effect the consistency of this rhythmicity.
The need the paper attempts to resolve is a critical one for the …
Reviewer #3 (Public review):
Summary:
The finding of rhythmic activity in the brain has, for a long time, engendered the theory of rhythmic modes of perception, that humans might oscillate between improved and worse perception depending on states of our internal systems. However, experiments looking for such modes have resulted in conflicting findings, particularly in those where the stimulus itself is not rhythmic. This paper seeks to take a comprehensive look at the effect and various experimental parameters which might generate these competing findings: in particular, the presentation of the stimulus to one ear or the other, the relevance of motor involvement, attentional demands, and memory: each of which are revealed to effect the consistency of this rhythmicity.
The need the paper attempts to resolve is a critical one for the field. However, as presented, I remain unconvinced that the data would not be better interpreted as showing no consistent rhythmic mode effect. It lacks a conceptual framework to understand why effects might be consistent in each ear but at different frequencies and only for some tasks with slight variants, some affecting sensitivity and some affecting bias.
Strengths:
The paper is strong in its experimental protocol and its comprehensive analysis, which seeks to compare effects across several analysis types and slight experiment changes to investigate which parameters could affect the presence or absence of an effect of rhythmicity. The prescribed nature of its hypotheses and its manner of setting out to test them is very clear, which allows for a straightforward assessment of its results
Weaknesses:
There is a weakness throughout the paper in terms of establishing a conceptual framework both for the source of "rhythmic modes" and for the interpretation of the results. Before understanding the data on this matter, it would be useful to discuss why one would posit such a theory to begin with. From a perceptual side, rhythmic modes of processing in the absence of rhythmic stimuli would not appear to provide any benefit to processing. From a biological or homeostatic argument, it's unclear why we would expect such fluctuations to occur in such a narrow-band way when neither the stimulus nor the neurobiological circuits require it.
Secondly, for the analysis to detect a "rhythmic mode", it must assume that the phase of fluctuations across an experiment (i.e., whether fluctuations are in an up-state or down-state at onset) is constant at stimulus onset, whereas most oscillations do not have such a total phase-reset as a result of input. Therefore, some theoretical positing of what kind of mechanism could generate this fluctuation is critical toward understanding whether the analysis is well-suited to the studied mechanism.
Thirdly, an interpretation of why we should expect left and right ears to have distinct frequency ranges of fluctuations is required. There are a large number of statistical tests in this paper, and it's not clear how multiple comparisons are controlled for, apart from experiment 4 (which specifies B&H false discovery rate). As such, one critical method to identify whether the results are not the result of noise or sample-specific biases is the plausibility of the finding. On its face, maintaining distinct frequencies of perception in each ear does not fit an obvious conceptual framework.
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Author response:
We are grateful to the reviewers for their extensive and constructive feedback. In large the three reviewers noted the following main points:
(1) The overall evidence for any rhythmicity in this data is not ‘very strong’.
We do agree and will tone down the conclusions accordingly. However, as one of the reviewers noted, a qualitative interpretation of the specific statistical results remains somewhat vague and speculative by necessity.
(2) The differences between the results for the individual experiments are generally small. Yet, the same reviewer also asks for speculations as to how differences between experiments can be interpreted.
We will consider these, but also note that a clear demonstration of the robustness of specific effects requires the replication of individual experiments in a separate experiment.
(3)…
Author response:
We are grateful to the reviewers for their extensive and constructive feedback. In large the three reviewers noted the following main points:
(1) The overall evidence for any rhythmicity in this data is not ‘very strong’.
We do agree and will tone down the conclusions accordingly. However, as one of the reviewers noted, a qualitative interpretation of the specific statistical results remains somewhat vague and speculative by necessity.
(2) The differences between the results for the individual experiments are generally small. Yet, the same reviewer also asks for speculations as to how differences between experiments can be interpreted.
We will consider these, but also note that a clear demonstration of the robustness of specific effects requires the replication of individual experiments in a separate experiment.
(3) A clear-cut interpretation of the current experimental design in the context of continuous listening and true vigilance tasks remains difficult. This makes the interpretation and generalization of the results difficult.
We do agree in principle, but also note that task designs very widely in previous work, which may be one reason for why there is no clear consensus on the existence or absence of a rhythmic mode of listening. We will consider specific suggestions for future work to be included in the revision.
(4) The adjustment of task difficulty in the present task design may pose a challenge. Reviewers also suggest analyzing potential rhythmicity in this task difficulty parameter.
We will consider this for the revision.
(5) A more clear-cut interpretation of what potential differences in the rhythmicity of sensitivity and bias would mean should be included.
We will provide this in the revision.
(6) The study should provide a stronger conceptual framework both for the source of "rhythmic modes" and why one may expect differences between ears.
In large this has been put forward by many previous studies testing and reporting rhythmicity in auditory tasks. Rhythmicity is pervasive in neural activity, but whether and how this relates to behavioral data remains less clear. These points will be clarified in a revision.
(7) Parallels to work in the visual domain by Fiebelkorn, Landau & Fries should be included.
We will discuss similarities and differences between studies on perceptual rhythmicity in the visual and auditory domains.
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