Instructions and experiential learning have similar impacts on pain and pain-related brain responses but produce dissociations in value-based reversal learning
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Evaluation Summary:
This paper is of potential interest to cognitive neuroscientists seeking to understand commonalities and differences in the neural basis of instructed and experiential reversal learning in the context of human pain. The authors report that learning from instructions versus experience leads to differences in the behavioral ratings of and the neural responses to noxious stimuli. The innovative experimental design and analyses in this study offer new perspectives on using neuro-computational models for understanding how explicitly informed vs experientially acquired information influences learning about cues predicting painful stimuli.
(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 #3 agreed to share their name with the authors.)
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Abstract
Recent data suggest that interactions between systems involved in higher order knowledge and associative learning drive responses during value-based learning. However, it is unknown how these systems impact subjective responses, such as pain. We tested how instructions and reversal learning influence pain and pain-evoked brain activation. Healthy volunteers (n=40) were either instructed about contingencies between cues and aversive outcomes or learned through experience in a paradigm where contingencies reversed three times. We measured predictive cue effects on pain and heat-evoked brain responses using functional magnetic resonance imaging. Predictive cues dynamically modulated pain perception as contingencies changed, regardless of whether participants received contingency instructions. Heat-evoked responses in the insula, anterior cingulate, and other regions updated as contingencies changed, and responses in the prefrontal cortex mediated dynamic cue effects on pain, whereas responses in the brainstem’s rostroventral medulla (RVM) were shaped by initial contingencies throughout the task. Quantitative modeling revealed that expected value was shaped purely by instructions in the Instructed Group, whereas expected value updated dynamically in the Uninstructed Group as a function of error-based learning. These differences were accompanied by dissociations in the neural correlates of value-based learning in the rostral anterior cingulate, thalamus, and posterior insula, among other regions. These results show how predictions dynamically impact subjective pain. Moreover, imaging data delineate three types of networks involved in pain generation and value-based learning: those that respond to initial contingencies, those that update dynamically during feedback-driven learning as contingencies change, and those that are sensitive to instruction. Together, these findings provide multiple points of entry for therapies designs to impact pain.
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Evaluation Summary:
This paper is of potential interest to cognitive neuroscientists seeking to understand commonalities and differences in the neural basis of instructed and experiential reversal learning in the context of human pain. The authors report that learning from instructions versus experience leads to differences in the behavioral ratings of and the neural responses to noxious stimuli. The innovative experimental design and analyses in this study offer new perspectives on using neuro-computational models for understanding how explicitly informed vs experientially acquired information influences learning about cues predicting painful stimuli.
(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. …
Evaluation Summary:
This paper is of potential interest to cognitive neuroscientists seeking to understand commonalities and differences in the neural basis of instructed and experiential reversal learning in the context of human pain. The authors report that learning from instructions versus experience leads to differences in the behavioral ratings of and the neural responses to noxious stimuli. The innovative experimental design and analyses in this study offer new perspectives on using neuro-computational models for understanding how explicitly informed vs experientially acquired information influences learning about cues predicting painful stimuli.
(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 #3 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
In humans, aversive associative learning occurs through experience or instruction. In this paper the authors examined how instructed and directly experienced aversive learning and reversal impacted subjective pain and used fMRI to study the neural systems underlying these processes. They identified cortical and striatal regions which followed reversals and thalamic and midbrain regions which maintained the original learning contingencies. They then used quantitative modeling to show that expected value changed more quickly with instructions compared with experiential learning and revealed a dissociation in the brain regions whose activity was correlated with these processes.
These results extend previous work from this group on instructed learning during fear conditioning into the subjective experience of …
Reviewer #1 (Public Review):
In humans, aversive associative learning occurs through experience or instruction. In this paper the authors examined how instructed and directly experienced aversive learning and reversal impacted subjective pain and used fMRI to study the neural systems underlying these processes. They identified cortical and striatal regions which followed reversals and thalamic and midbrain regions which maintained the original learning contingencies. They then used quantitative modeling to show that expected value changed more quickly with instructions compared with experiential learning and revealed a dissociation in the brain regions whose activity was correlated with these processes.
These results extend previous work from this group on instructed learning during fear conditioning into the subjective experience of pain and the effects of expectation on this. However, the methods used for analyzing the data are not described in enough detail for this reviewer to understand what the BOLD signal is integrating in the different analyses. More broadly, there are important differences found in the brain regions mediating instructed vs. directly experienced aversive learning between this study and previous work. The reasons for these differences are unclear and without a deeper understanding of these differences the impact of this line of research and the potential impact of the current paper could be compromised. If the reasons for these differences could be addressed in some conceptual way, the current paper could be much more compelling.
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Reviewer #2 (Public Review):
The study sets out to compare behavioural and neural measures of instructed and experiential reversal learning in health volunteers. The results identified brain regions with distinct response patterns that partly dependent on the type of learning. The exploration of differences between instructed and experiential learning is of great importance - from a general learning perspective but even more so because of its immediate clinical relevance. The study is well designed, the analysis is sound, and the complex findings are presented with a clear structure. I would particularly like to commend the authors for their diligent reporting of both Bayesian and frequentist statistics which allows the reader to assess the findings and their relevance in detail. However, I have concerns regarding the robustness of the …
Reviewer #2 (Public Review):
The study sets out to compare behavioural and neural measures of instructed and experiential reversal learning in health volunteers. The results identified brain regions with distinct response patterns that partly dependent on the type of learning. The exploration of differences between instructed and experiential learning is of great importance - from a general learning perspective but even more so because of its immediate clinical relevance. The study is well designed, the analysis is sound, and the complex findings are presented with a clear structure. I would particularly like to commend the authors for their diligent reporting of both Bayesian and frequentist statistics which allows the reader to assess the findings and their relevance in detail. However, I have concerns regarding the robustness of the data and the interpretation of the findings.
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Reviewer #3 (Public Review):
Atlas and colleagues use a reversal-learning task in which two auditory cues predict painful heat stimuli calibrated to three levels of intensity. One group of participants (n=20) and is not informed about the initial contingencies and about the reversals, whereas a second group of participants (n=20) is explicitly instructed about the initial contingencies and about the reversals. The authors provide detailed and sound analyses of behavioral ratings of subjective pain intensity and pain expectations as well as (mediation) analyses of fMRI signals during the receipt of painful stimuli. I find it laudable that the authors use Rescorla-Wagner (RW) models, which are very common in studies on appetitive learning and have also been used in studies on aversive learning.
In my view, one of the most interesting …
Reviewer #3 (Public Review):
Atlas and colleagues use a reversal-learning task in which two auditory cues predict painful heat stimuli calibrated to three levels of intensity. One group of participants (n=20) and is not informed about the initial contingencies and about the reversals, whereas a second group of participants (n=20) is explicitly instructed about the initial contingencies and about the reversals. The authors provide detailed and sound analyses of behavioral ratings of subjective pain intensity and pain expectations as well as (mediation) analyses of fMRI signals during the receipt of painful stimuli. I find it laudable that the authors use Rescorla-Wagner (RW) models, which are very common in studies on appetitive learning and have also been used in studies on aversive learning.
In my view, one of the most interesting findings of this study is a difference between the uninstructed and the instructed groups of participants in the relation between signals in the rostral anterior cingulate cortex (rACC) and the expected value of painful stimuli (see Figure 7). One strength of this paper is that this finding of a differential involvement of the rACC between uninstructed and the instructed learning situations might give a better idea of the general role of the rACC. This can inspire new studies that test the generality of the reported finding in a rather straightforward way by using different types of aversive and appetitive stimuli as well as different types of instructions and contingencies between cues and stimuli.
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