Consilience in the Peripheral Sensory Adaptation Response

  1. Willy Wong

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Abstract

Measurements of the peripheral sensory adaptation response were compared to a simple mathematical relationship involving the spontaneous, peak and steady-state activities. This relationship is based on the geometric mean and is found to be obeyed to good approximation in peripheral sensory units showing a sustained response to prolonged stimulation. From an extensive review of past studies, the geometric mean relationship is shown to be independent of modality and is satisfied in a wide range of animal species. The consilience of evidence, from nearly one hundred years of experiments beginning with the work of Edgar Adrian, suggests that this is a fundamental result of neurophysiology.

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  1. eLife

    ###Reviewer #4:

    The author investigated the relationship between spontaneous (SR), peak (PR), and steady-state (SS) firing rate in sensory neurons (across modalities) by extracting data from approximately ten studies, published between 1928 and 2017. The relationship between SR, PR, and SS is surprisingly simple: SS =sqrt(PRxSR). The author concludes that this is a universal law of sensory adaptation.

    General Assessment: The claims of universality are not supported by the analysis.

    Major comments: The primary claim of a universal law of adaptation is based on a meta-analysis of fewer than 20 several hand-picked papers. This is contrary to good scientific practice of meta-analyses. To truly assess the universality of the rule, the author should define a time period, a set of journals, and possibly some other criteria for exclusion/inclusion and then study the relationship across all publications that meet these criteria. Without such a clearly defined approach, the reader cannot know whether the examples were cherry-picked.

    The comparisons of (extracted) experimental data and the model are entirely "by eye"; statistical analysis is lacking.

    Even within the chosen sample, universality is clearly a step too far and the author's explanations of why the universal law fails are not particularly convincing ("the visual system is complex"). There may be something to the claim that the law only applies "in the absence of interaction from others cells in the neural circuitry", but this should be part of the study (i.e investigate only those papers that studied neurons that were isolated in this sense), not as an ad-hoc explanation of discrepancies.

    The manuscript only states the "universal law" but leaves an explanation to future work. This is unsatisfactory. Detailed neuronal models exist that explain adaptation (e.g. in terms of the opening of potassium channels). These alternative biophysical explanations need to be considered.

  2. eLife

    ###Reviewer #3:

    This manuscript by Wong proposes that steady state responses to a constant sensory stimulus-the responses observed after adaptation-are well predicted by a simple relationship between the spontaneous firing rate and the peak firing rate, namely their geometric mean. The author provides evidence extracted from measurements made in previous published studies, across species and modalities.

    The paper presents a simple and somewhat interesting observation. However, it is difficult to accept the claim and support publication for several reasons:

    1. The comparisons between the predicted and measured responses are entirely qualitative, and there is no alternative model considered. The predictions in Table 1 are pretty good but in many cases the arithmetic mean works reasonably as well (unless peak rates are very high). The steady state will lie somewhere between peak and spontaneous. Where is the quantitative evidence that the geometric mean is better than an alternative? What other relationships might better map the quantities on to each other?

    2. There is little context for the observation: if true, why should we care that Eq 1,2 hold? The discussion hints that the observation is consistent with theoretical principles. If this were laid out in a compelling way, it would greatly increase the impact and relevance of the observation. As it stands, the observation has little context. The implications are unclear.

    3. It is not clear how the studies considered here (i.e. where the data came from) were chosen. Surely there are many studies of sensory responses to the constant stimuli. How did the author choose this small subset (~10 studies)? For a 'universal' law, one would want to see many studies considered. In addition, in the studies considered here, the values were extracted in an ad hoc manner.

    4. The discussion points out many cases in which the rule does not apply (whenever neurons are embedded in a circuit as opposed to being primary sensory neurons). This limits the appeal of the proposal, unless one can provide theory/explanation for why such a relationship should hold in the periphery but not in more central structures.

    5. Previous work has dispelled the notion of a steady state response, arguing that responses continue to decrease with adaptation duration, following a power law dependence (Drew and Abbott, 2006, J Neurophysiol 96: 826). If so, the rule proposed here is unlikely to hold across adaptation duration, again suggesting they are not broadly applicable.

  3. eLife

    ###Reviewer #2:

    This paper proposes a universal law of adaptation that occurs during sustained sensory stimulation. The law states that the sustained response of sensory afferents equals the square root of the product of the spontaneous and transient, peak response. The author shows several examples of previously published results to support the claim, some dating back to the seminal studies by Adrian. The author states that the law can be derived from a theory of sensory processing but does not provide further information on this (he refers to a publication in preparation).

    This is interesting work and the paper is well-written. However, I am not convinced by this claim of a universal law of adaptation. First, it does not appear to be universal, and, second, the empirical data that are provided to support its universality are not convincing yet.

    1. The law is not universal: in his Discussion, the author lists exceptions to the rule, in the visual system, auditory system and even for somatosensory afferents. Explanations are given of why the law does not hold in some of these cases, but the exceptions show that the law is not universal. Even when it is not universal, the theory should be able to predict in which cases it holds and when it does not hold.

    2. I am not convinced by the evidence presented in Figure 2. In several instances, the slope of the relationship between the log peak and log sustained (steady state) activity does not seem to be equal to the predicted 1/2: e.g. in panels b and c .The author should have computed the slope and tested whether it was 1/2.

  4. eLife

    ###Reviewer #1:

    This study reports an interesting observation, namely that the firing rate after sensory adaptation appears to be equal to the geometric mean of the peak firing rate and the spontaneous firing rate. However, there are concerns about the theoretical motivation and general empirical evidence supporting this observation.

    1. Theoretical motivation: still unclear even after discussion, although we are told it exists. "The derivation of Eqs 1-2 of will be the subject of a later publication."

    2. Is this relationship supposed to hold for each stimulation or on average? The author seems to be only working with averages.

    It is not clear why exactly these (quite old) studies were selected. What was the criteria to include these studies in the meta-analysis? A number of exceptions are later discussed however.

    Alternative of in-depth analysis of existing datasets requested from other authors was explicitly not done. Could also address the trial-wise validity.

    "Not only does adaptation show time-varying changes in firing rate, but the variability makes it difficult to know exactly which value to choose. Averaging the data is not feasible without extracting a large number of data points, and this was not possible from noisy images. As such, with the exception of two studies, ... a visual estimation of the average activity in the final portion of the adaptation curve was used."

    The error introduced by visual estimation remains unknown.

    1. Counter-example in one of the few easily accessible papers, in the ferret, reference 16 (https://pubmed.ncbi.nlm.nih.gov/22694786/#&gid=article-figures&pid=fig-6-uid-5 ). Another counterexample appears in Fig 8 of this randomly chosen paper, although maybe the mechanoreceptor of the cricket doesn't count due to some exclusion criterion, since it is an interneuron. (https://journals.physiology.org/doi/full/10.1152/jn.1997.77.1.207?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub 0pubmed)

    2. The law doesn't hold for a number of exceptions, this is not announced until the discussion (missing in abstract).

    3. The discussion ignores existing literature on information content and possible function of the sustained response, and of adaptation in general (e.g. gain control).

    4. Introduction: failure to cite recent reviews on this topic, e.g. "has been repeated many times.... More modern methodologies..." cites nothing after 1970s.

    5. At which time point is the relationship supposed to hold true? What happens when stimulation time becomes very long? Does the firing rate reach steady state in all of these studies?

  5. eLife

    ##Preprint Review

    This preprint was reviewed using eLife’s Preprint Review service, which provides public peer reviews of manuscripts posted on bioRxiv for the benefit of the authors, readers, potential readers, and others interested in our assessment of the work. This review applies only to version 2 of the manuscript.

  6. Version published to 10.1101/2020.02.17.953448 on bioRxiv