A single exposure to altered auditory feedback causes observable sensorimotor adaptation in speech
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Evaluation Summary:
The paper demonstrates the adaptation of speech after a single trial of perturbing the fundamental frequency of an utterance. The findings confirm existing theories of speech adaptation, but constitute an important missing piece of evidence in the current literature.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Abstract
Sensory errors induce two types of behavioral changes: rapid compensation within a movement and longer-term adaptation of subsequent movements. Although adaptation is hypothesized to occur whenever a sensory error is perceived (including after a single exposure to altered feedback), adaptation of articulatory movements in speech has only been observed after repeated exposure to auditory perturbations, questioning both current theories of speech sensorimotor adaptation and the universality of more general theories of adaptation. We measured single-exposure or ‘one-shot’ learning in a large dataset in which participants were exposed to intermittent, unpredictable perturbations of their speech acoustics. On unperturbed trials immediately following these perturbed trials, participants adjusted their speech to oppose the preceding shift, demonstrating that learning occurs even after a single exposure to auditory error. These results provide critical support for current theories of sensorimotor adaptation in speech and align speech more closely with learning in other motor domains.
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Author Response
Reviewer #2 (Public Review):
The basic idea of assessing whether adaptive responses in speech learning mirror those observed in upper limb movements is appealing. However, there are a number of concerns regarding the present paper. First, the perturbations which are used are unpredictable and hence unlearnable. From work on upper limb movement, it is known that when subjects are presented with unlearnable perturbations, their response is adaptive but different than that observed in response to learnable perturbations. With unpredictable perturbations subjects cocontract to resist limb displacement whereas a directional response is observed when the perturbation is predictable. Although compensation is present here in response to unpredictable perturbations, whether it matches that which occurs in learning is …
Author Response
Reviewer #2 (Public Review):
The basic idea of assessing whether adaptive responses in speech learning mirror those observed in upper limb movements is appealing. However, there are a number of concerns regarding the present paper. First, the perturbations which are used are unpredictable and hence unlearnable. From work on upper limb movement, it is known that when subjects are presented with unlearnable perturbations, their response is adaptive but different than that observed in response to learnable perturbations. With unpredictable perturbations subjects cocontract to resist limb displacement whereas a directional response is observed when the perturbation is predictable. Although compensation is present here in response to unpredictable perturbations, whether it matches that which occurs in learning is uncertain. It is hard to know whether responses to unpredictable speech perturbations can serve as a model to understand the adaptation that occurs during learning. This would seem important in the present context where the goal is to understand the structure of sequential dependencies in learning.
We agree that differences exist between adaptive responses to consistent vs. inconsistent perturbations, particularly in studies with mechanical perturbations of the limb. Random perturbations very similar to those used here have been used extensively in the reaching literature studying one-shot learning, especially when the error is purely sensory (i.e. when visual feedback is perturbed), taking co-contractions due to limb displacement out of the equation. The current study has a similar advantage in avoiding the possibility of stiffening/co-contraction as an adaptive strategy, and does show that even inconsistent sensory errors can elicit measurable directional responses. We agree that the magnitude of this one-shot adaptation may underestimate the adaptation seen in when perturbations are consistent across trials; a brief discussion of these points has been added (lines 159-165).
A further concern is the magnitude of the on-line compensation response and the adaptation response observed in the following movement. While there are statistical differences in the magnitudes of responses to upward and downward shifts in auditory feedback, neither response alone appears to be different than zero, nor are these specific tests reported. It is hard to draw any conclusion from non-zero responses.
We now report differences from 0: the adaptation response was significantly different from 0 in the pre-defined time window for post-up trials. The response was numerically but not significantly larger than 0 in this time window for post-down trials; however, a cluster-based permutation analysis of all time points across the syllable yielded significant differences from 0 in both post-up and post-down conditions (see new horizontal bars on Fig. 2A). This is described in the results in lines 120-122 and in the methods in lines 263-266 and 295-297.
The claim that on-line compensation responses and the frequency shifts associated with the subsequent utterance are based on separate mechanisms rests on the absence of a relationship between these variables. However, it is difficult to know what to conclude when a relationship is absent. One might suspect that part of the reason for the null relationship is that all perturbations in the present study were all more or less equal in magnitude. Accordingly, variations in both the compensatory response and the response on the subsequent trial may effectively be noise. A more convincing demonstration might involve the use of perturbations of different magnitudes. One would be more inclined to find the absence of a relationship between the variables of interest more informative if there was no relationship under these conditions.
We now present further evidence for a trial-level relationship between compensation and adaptation using a test on the distribution of correlation coefficients across individuals, replacing our Monte Carlo simulation (see response to Reviewer 1 above). We have amended our explanation and discussion in lines 133-139 & 166-177. We recast these conflicting results (no main effect of compensation on adaptation, but a significant tendency for correlation within individuals) as mixed results that do not rule out a direct feedforward relationship; however, there is a stronger burden on models that have a reliance on this trial-level relationship to show that it is reliably predictive of adaptive behavior. We agree that datasets with parametrically varying perturbation size (within the same participants) would allow for a more controlled elicitation of variability in compensation responses and may shed more light on the individual relationship.
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Evaluation Summary:
The paper demonstrates the adaptation of speech after a single trial of perturbing the fundamental frequency of an utterance. The findings confirm existing theories of speech adaptation, but constitute an important missing piece of evidence in the current literature.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
The demonstration of single trial adaptation in speech is a very useful addition to the existing literature. It confirms, rather than challenge, existing theories - but it is an important finding nonetheless. The authors also provide a good estimate of the size of the effect. The relationship between the online compensation and adaptation cannot not decisively decide between feedback-command-based and prediction-error based models of adaptation given the somewhat mixed results (different relationship within- and across-subjects). In either case, the analysis does not provide a strong test of these hypothesis, as either outcome would be consistent with a prediction-error (or internal model) based explanation.
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Reviewer #2 (Public Review):
This paper reports a re-analysis of data from six previous studies by the same authors, in which patterns of compensation are assessed in response to unexpected perturbations of auditory feedback in speech. The focus is on the relationship between the magnitude of the on-line vocal compensatory response and the characteristics of the acoustical change during the production of an immediately following unperturbed utterance. It is found that participants produce an on-line response which opposes the perturbation; if auditory feedback is perturbed upward in frequency, a relatively short latency shift in the frequency composition of the vocal output is observed in the opposite direction. On the following unperturbed trial, a shift in the frequency of the vocal output is observed that is likewise opposite to the …
Reviewer #2 (Public Review):
This paper reports a re-analysis of data from six previous studies by the same authors, in which patterns of compensation are assessed in response to unexpected perturbations of auditory feedback in speech. The focus is on the relationship between the magnitude of the on-line vocal compensatory response and the characteristics of the acoustical change during the production of an immediately following unperturbed utterance. It is found that participants produce an on-line response which opposes the perturbation; if auditory feedback is perturbed upward in frequency, a relatively short latency shift in the frequency composition of the vocal output is observed in the opposite direction. On the following unperturbed trial, a shift in the frequency of the vocal output is observed that is likewise opposite to the direction of the original perturbation. The authors find that the across subjects there is a small but significant correlation in the magnitude of the initial online compensation response and the so-called one-shot adaptation on the subsequent trial; subjects that show larger compensatory responses also show greater adaptation on the following trial. The authors attribute this pattern to individual differences between subjects. When this same relationship is examined on a trial-to-trial basis no correlation is observed.
The basic idea of assessing whether adaptive responses in speech learning mirror those observed in upper limb movements is appealing. However, there are a number of concerns regarding the present paper. First, the perturbations which are used are unpredictable and hence unlearnable. From work on upper limb movement, it is known that when subjects are presented with unlearnable perturbations, their response is adaptive but different than that observed in response to learnable perturbations. With unpredictable perturbations subjects cocontract to resist limb displacement whereas a directional response is observed when the perturbation is predictable. Although compensation is present here in response to unpredictable perturbations, whether it matches that which occurs in learning is uncertain. It is hard to know whether responses to unpredictable speech perturbations can serve as a model to understand the adaptation that occurs during learning. This would seem important in the present context where the goal is to understand the structure of sequential dependencies in learning.
A further concern is the magnitude of the on-line compensation response and the adaptation response observed in the following movement. While there are statistical differences in the magnitudes of responses to upward and downward shifts in auditory feedback, neither response alone appears to be different than zero, nor are these specific tests reported. It is hard to draw any conclusion from non-zero responses.
The claim that on-line compensation responses and the frequency shifts associated with the subsequent utterance are based on separate mechanisms rests on the absence of a relationship between these variables. However, it is difficult to know what to conclude when a relationship is absent. One might suspect that part of the reason for the null relationship is that all perturbations in the present study were all more or less equal in magnitude. Accordingly, variations in both the compensatory response and the response on the subsequent trial may effectively be noise. A more convincing demonstration might involve the use of perturbations of different magnitudes. One would be more inclined to find the absence of a relationship between the variables of interest more informative if there was no relationship under these conditions.
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