Evidence accumulation, not ‘self-control’, explains dorsolateral prefrontal activation during normative choice
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Evaluation Summary:
This paper will be of interest to neuroscientists studying decision-making and the frontal lobe. The paper combines computational modeling with brain imaging across several datasets to better understand the role of brain regions previously implicated in self-control during normative behavior (generosity, healthy eating). On balance, the data provide more support for the view that dorsolateral prefrontal cortex is involved in reading out the evidence in favor of different choice alternatives than the view that this region implements control processes that bias choices towards normative goals.
(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. The reviewers remained anonymous to the authors.)
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Abstract
What role do regions like the dorsolateral prefrontal cortex (dlPFC) play in normative behavior (e.g., generosity, healthy eating)? Some models suggest that dlPFC activation during normative choice reflects controlled inhibition or modulation of default hedonistic preferences. Here, we develop an alternative account, showing that evidence accumulation models predict trial-by-trial variation in dlPFC response across three fMRI paradigms and two self-control contexts (altruistic sacrifice and healthy eating). Using these models to simulate a variety of self-control dilemmas generated a novel prediction: although dlPFC activity might typically increase for norm-consistent choices, deliberate self-regulation focused on normative goals should decrease or even reverse this pattern (i.e., greater dlPFC response for hedonistic, self-interested choices). We confirmed these predictions in both altruistic and dietary choice contexts. Our results suggest that dlPFC response during normative choice may depend more on value-based evidence accumulation than inhibition of our baser instincts.
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Reviewer #3 (Public Review):
In this manuscript, Hutcherson and Tusche investigate the role of the DLPFC in normative behavior. Challenging some standard accounts, they propose that the DLPFC response track a value-based evidence accumulation process. This claim is supported by qualitative computational simulations - of a an attribute-based neural drift diffusion model aka anDDM), and a model-based reanalysis of three fMRI studies.
Overall, I find the theoretical proposal quite convincing: the model makes sense, and seem to account pretty well for the behavioral data (choices and reaction times) in several experiments and decision contexts. Yet, the computational model (anDDM) seems close to the one previously used in (Tusche and Hutcherson, 2018). I am really sympathetic to the authors' approach (testing a well formulated computational …
Reviewer #3 (Public Review):
In this manuscript, Hutcherson and Tusche investigate the role of the DLPFC in normative behavior. Challenging some standard accounts, they propose that the DLPFC response track a value-based evidence accumulation process. This claim is supported by qualitative computational simulations - of a an attribute-based neural drift diffusion model aka anDDM), and a model-based reanalysis of three fMRI studies.
Overall, I find the theoretical proposal quite convincing: the model makes sense, and seem to account pretty well for the behavioral data (choices and reaction times) in several experiments and decision contexts. Yet, the computational model (anDDM) seems close to the one previously used in (Tusche and Hutcherson, 2018). I am really sympathetic to the authors' approach (testing a well formulated computational theory on several datasets), and to the proposition that DLPFC's role in decision making might be actually much more "downstream" (i.e. response selection stage) than usually assumed. In that respect, this paper could have a nice impact in the field of neuroeconomics/decision neuroscience. I am, however, less convinced by the second step of the demonstration - i.e. the translation of the model in terms of brain activity and the neuroimaging analyses.
My main concern is that, although I am quite convinced that the anDDM accounts well for behavior, I find very unclear what the predicted activity (the sum of neural activation across the two pools over the decision time) accounts for - or could be confounded with. In short, the predicted activity seems to closely correspond to - and correlate with - a linear transformation of %choice and/or RT (see Figure 2 and Figure S1) . This raises several important questions/concerns.
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Reviewer #2 (Public Review):
I am sympathetic to the views presented in the paper and I believe there is definitely merit to what the authors are claiming. I also appreciate the combination of computational modeling and fMRI. I do somewhat question the novelty of the findings and think that there are other, related, interpretations of the results that the authors could discuss. No individual study provides sufficient evidence for the authors' conclusions. However, that is the benefit of this mini meta-analysis. There are potentially other explanations for the authors' results, such as the DLPFC becoming active when subjects disobey experimenters' instructions, though perhaps the correlation of the DLPFC with accumulated evidence assuages this concern. Overall I think this is an interesting, compelling study, but it could benefit from …
Reviewer #2 (Public Review):
I am sympathetic to the views presented in the paper and I believe there is definitely merit to what the authors are claiming. I also appreciate the combination of computational modeling and fMRI. I do somewhat question the novelty of the findings and think that there are other, related, interpretations of the results that the authors could discuss. No individual study provides sufficient evidence for the authors' conclusions. However, that is the benefit of this mini meta-analysis. There are potentially other explanations for the authors' results, such as the DLPFC becoming active when subjects disobey experimenters' instructions, though perhaps the correlation of the DLPFC with accumulated evidence assuages this concern. Overall I think this is an interesting, compelling study, but it could benefit from more evidence on the correspondence between behavior and brain activity.
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Reviewer #1 (Public Review):
Hutcherson and Tusche address an important question: what is the role of dorsolateral prefrontal cortex in normative decision-making? Some have argued that dlPFC plays a role akin to cognitive control - overriding non-normative choices or holding in mind and enhancing the weight of normative goals. Others have argued that dlPFC reflects the accumulation of evidence, akin to a drift diffusion process, during decision-making, and that any apparent special role in normative choices follows from this. Hutcherson and Tusche provide evidence in favor of the second view from three neuroimaging studies across two domains where norms are relevant (altruistic choice and healthy food choice). The key prediction that distinguishes the evidence accumulation hypothesis is that, when normative considerations are weighted …
Reviewer #1 (Public Review):
Hutcherson and Tusche address an important question: what is the role of dorsolateral prefrontal cortex in normative decision-making? Some have argued that dlPFC plays a role akin to cognitive control - overriding non-normative choices or holding in mind and enhancing the weight of normative goals. Others have argued that dlPFC reflects the accumulation of evidence, akin to a drift diffusion process, during decision-making, and that any apparent special role in normative choices follows from this. Hutcherson and Tusche provide evidence in favor of the second view from three neuroimaging studies across two domains where norms are relevant (altruistic choice and healthy food choice). The key prediction that distinguishes the evidence accumulation hypothesis is that, when normative considerations are weighted more strongly (for example, due to regulatory focus instructions), non-normative choices should be associated with stronger activation than normative ones. The authors observe moderate support for this prediction.
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Evaluation Summary:
This paper will be of interest to neuroscientists studying decision-making and the frontal lobe. The paper combines computational modeling with brain imaging across several datasets to better understand the role of brain regions previously implicated in self-control during normative behavior (generosity, healthy eating). On balance, the data provide more support for the view that dorsolateral prefrontal cortex is involved in reading out the evidence in favor of different choice alternatives than the view that this region implements control processes that bias choices towards normative goals.
(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. The reviewers remained anonymous to the authors.)
Evaluation Summary:
This paper will be of interest to neuroscientists studying decision-making and the frontal lobe. The paper combines computational modeling with brain imaging across several datasets to better understand the role of brain regions previously implicated in self-control during normative behavior (generosity, healthy eating). On balance, the data provide more support for the view that dorsolateral prefrontal cortex is involved in reading out the evidence in favor of different choice alternatives than the view that this region implements control processes that bias choices towards normative goals.
(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. The reviewers remained anonymous to the authors.)
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