Individual differences in internal oscillator properties that impact perception and production of rhythms

Reviewer #1 (Public Review):

Summary:
This study assumes and weakly tests that auditory rhythm processing is produced by internal oscillating systems, and it evaluates the properties of such putative oscillators across individuals. The authors designed an experiment and performed analyses that address individuals' preferred rate and flexibility, with a special focus on how much past rhythms influence subsequent trials. They find evidence for such historical dependence and show that we adapt less well to new rhythms as we age. While I have important doubts about the entrainment-based interpretation of the results, this work offers a useful contribution to our understanding of individual differences in rhythm processing regardless.

Strengths:
The inclusion of two tasks -- a tapping and a listening task -- complement each other methodologically. By analysing both the production and tracking of rhythms, the authors emphasize the importance of the characteristics of the receiver, the external world, and their interplay. The relationship between the two tasks and components within tasks are explored using a range of analyses. The visual presentation of the results is very clear. The age-related changes in flexibility are useful and compelling.

Weaknesses:
At times, I found it challenging to evaluate the scientific merit of this study from what was provided in the introduction and methods. It is not clear what the experiment assumes, what it evaluates, and which competing accounts or predictions are at play. While some of these questions are answered, clear ordering and argumentative flow is lacking. With that said, I found the Abstract and General Discussion much clearer, and I would recommend reformulating the early part of the manuscript based on the structure of those segments.

Second, in my reading, it is not clear to what extent the study assumes versus demonstrates the entrainment of internal oscillators. I find the writing somewhat ambiguous on this count: on the one hand, an entrainment approach is assumed a priori to design the experiment ("an entrainment approach is adopted") yet a primary result of the study is that entrainment is how we perceive and produce rhythms ("Overall, the findings support the hypothesis that an oscillatory system with a stable preferred rate underlies perception and production of rhythm..."). While one could design an experiment assuming X and find evidence for X, this requires testing competing accounts with competing hypotheses -- and this was not done.

In my view, more evidence is required to bolster the findings as entrainment-based regardless of whether that is an assumption or a result. Indeed, while the effect of previous trials into the behaviour of the current trial is compatible with entrainment hypotheses, it may well be compatible with competing accounts as well. And that would call into question the interpretation of results as uncovering the properties of oscillating systems and age-related differences in such systems. Thus, I believe more evidence is needed to bolster the entrainment hypothesis.

For example, a key prediction of the entrainment model -- which assumes internal oscillators as the mechanism of action -- is that behaviour in the SMT and PTT tasks follows the principles of Arnold's Tongue. Specifically, tapping and listening performance should worsen systematically as a function of the distance between the presented and preferred rate. On a participant-by-participant, does performance scale monotonically with the distance between the presented and preferred rate? Some of the analyses hint at this question, such as the effect of 𝚫IOI on accuracy, but a recontextualization, further analyses, or additional visualizations would be helpful to demonstrate evidence of a tongue-like pattern in the behavioural data. Presumably, non-oscillating models do not follow a tongue-like pattern, but again, it would be very instructive to explicitly discuss that.

Fourth, harmonic structure in behaviour across tasks is a creative and useful metric for bolstering the entrainment hypothesis specifically because internal oscillators should display a preference across their own harmonics. However, I have some doubts that the analyses as currently implemented indicate such a relationship. Specifically, the main analysis to this end involves summing the residuals of the data closest to y=x, y=2*x and y=x/2 lines and evaluating whether this sum is significantly lower than for shuffled data. Out of these three dimensions, y=x does not comprise a harmonic, and this is an issue because it could by itself drive the difference of summed residuals with the shuffled data. I am uncertain whether rerunning the same analysis with the x=y dimension excluded constitutes a simple resolution because presumably there are baseline differences in the empirical and shuffled data that do not have to do with harmonics that would leak into the analysis. To address this, a simulation with ground truths could be helpful to justify analyses, or a different analysis that evaluates harmonic structure could be thought of.

Reviewer #2 (Public Review):

Summary:
In the current work, authors deploy a set of behavioral tasks to explore individual differences in the preferred perceptual and motor rhythms. They found a consistent individual preference for a given perceptual and motor frequency across tasks and, while these were correlated, the latter is slower than the former one. Additionally, they show that the accuracy of adaptation to rate changes is proportional to the amount of rate variation and, crucially, the amount of adaptation decreases with age.

Strengths:
Authors carefully designed several experiments to measure individual preferred motor and perceptual tempo. Furthermore, before completing the main experiment they validated the experimental design by testing the consistency across tasks and test-retest. Additionally, to the value of the reported findings, the introduced paradigm represents a useful tool for future research.
The obtained data is rigorously analyzed using a diverse set of tools, each adapted to the specificities across the different research questions and tasks.
This study identifies several relevant behavioral features: (i) each individual shows a preferred and reliable motor and perceptual tempo and, while both are related, the motor is consistently slower than the pure perceptual one; (ii) the existence of hysteresis in the adaptation to rate variations; and (iii) the decrement of this adaptation with age. All these observations are valuable for the auditory-motor integration field of research, and they could potentially inform existing biophysical models to increase their descriptive power.

Weaknesses:
The current study is presented in the framework of the ongoing debate of oscillator vs. timekeeper mechanisms underlying perceptual and motor timing, and authors claim that the observed results support the former mechanism. In this line, every obtained result is related by the authors to a specific ambiguous (i.e., not clearly related to a biophysical parameter) feature of an internal oscillator. As pointed out by an essay on the topic (1), claiming that a pattern of results is compatible with an "oscillator" could be misleading, since some features typically used to validate or refute such mechanisms are not well grounded on real biophysical models. Relatedly, a recent study (2) shows that two quantitatively different computational algorithms (i.e., absolute vs relative timing) can be explained by the same biophysical model. This demonstrates that what could be interpreted as a timekeeper, or an oscillator can represent the same biophysical model working under different conditions. For this reason, if authors would like to argue for a given mechanism underlying their observations, they should include a specific biophysical model, and test its predictions against the observed behavior. For example, it's not clear why authors interpret the observation of the trial's response being modulated by the rate of the previous one, as an oscillator-like mechanism underlying behavior. As shown in (1) a simple oscillator returns to its natural frequency as soon as the stimulus disappears, which will not predict the long-lasting effect of the previous trial. Furthermore, a timekeeper-like mechanism with a long enough integration window is compatible with this observation.
Still, authors can choose to disregard this suggestion, and not testing a specific model, but if so, they should restrict this paper to a descriptive study of the timing phenomena.

1. Doelling, K. B., & Assaneo, M. F. (2021). Neural oscillations are a start toward understanding brain activity rather than the end. PLoS biology, 19(5), e3001234.
2. Doelling, K. B., Arnal, L. H., & Assaneo, M. F. (2022). Adaptive oscillators provide a hard-coded Bayesian mechanism for rhythmic inference. bioRxiv, 2022-06.