Functional gradients in the human lateral prefrontal cortex revealed by a comprehensive coordinate-based meta-analysis
Abstract
The lateral prefrontal cortex (LPFC) of humans enables flexible goal-directed behavior. However, its functional organization remains actively debated after decades of research. Moreover, recent efforts aiming to map the LPFC through meta-analysis are limited, either in scope or in the inferred specificity of structure-function associations. These limitations are in part due to the limited expressiveness of commonly-used data analysis tools, which restricts the breadth and complexity of questions that can be expressed in a meta-analysis. Here, we adopt NeuroLang, a novel approach to more expressive meta-analysis based on probabilistic first-order logic programming, to infer the organizing principles of the LPFC from 14,371 neuroimaging studies. Our findings reveal a rostrocaudal and a dorsoventral gradient, respectively explaining the most and second most variance in meta-analytic connectivity across the LPFC. Moreover, we identify a unimodal-to-transmodal spectrum of coactivation patterns along with a concrete-to-abstract axis of structure-function associations extending from caudal to rostral regions of the LPFC. Finally, we infer inter-hemispheric asymmetries along the principal rostrocaudal gradient, identifying hemisphere-specific associations with topics of language, memory, response inhibition, and sensory processing. Overall, this study provides a comprehensive meta-analytic mapping of the LPFC, grounding future hypothesis generation on a quantitative overview of past findings.
Data availability
All data and scripts used in this study are openly available to be accessed and freely used by the community. The source code of NeuroLang is freely available on GitHub at https://github.com/NeuroLang/NeuroLang.
Article and author information
Author details
Funding
European Research Council (10.3030/757672)
- Majd Abdallah
European Research Council (10.3030/757672)
- Demian Wassermann
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- David Badre, Brown University, United States
Ethics
Human subjects: The current study uses brain activation data from the Individual Brain Charting Dataset (IBC). In the original paper of IBC, the authors indicate that they received written consent from the subjects involved in the study. To quote from Pinho et al. Individual Brain Charting, a high-resolution fMRI dataset for cognitive mapping. Sci Data. 2018 : "The experimental procedures were approved by a regional ethical committee for medical protocols in Île-de-France ("Comité de Protection des Personnes" - no. 14-031) and a committee to ensure compliance with data-protection rules ("Commission Nationale de l'Informatique et des Libertés" - DR-2016-033). They were undertaken with the informed written consent of each participant according to the Helsinki declaration and the French public health regulation. Participants were reimbursed on the basis of 80 per MRI acquisition with extra-fees for any additional session."
Version history
- Received: January 10, 2022
- Preprint posted: January 23, 2022 (view preprint)
- Accepted: September 27, 2022
- Accepted Manuscript published: September 28, 2022 (version 1)
- Version of Record published: October 18, 2022 (version 2)
Copyright
© 2022, Abdallah et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.
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Our ability to recall details from a remembered image depends on a single mechanism that is engaged from the very moment the image disappears from view.