Functional gradients in the human lateral prefrontal cortex revealed by a comprehensive coordinate-based meta-analysis

  1. Majd Abdallah  Is a corresponding author
  2. Gaston E Zanitti
  3. Valentin Iovene
  4. Demian Wassermann  Is a corresponding author
  1. Inria Saclay - Île-de-France Research Centre, France

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.

The following previously published data sets were used

Article and author information

Author details

  1. Majd Abdallah

    Inria Saclay - Île-de-France Research Centre, Palaiseau, France
    For correspondence
    majd.abdallah@inria.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8371-1793
  2. Gaston E Zanitti

    Inria Saclay - Île-de-France Research Centre, Palaiseau, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5549-9548
  3. Valentin Iovene

    Inria Saclay - Île-de-France Research Centre, Palaiseau, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Demian Wassermann

    Inria Saclay - Île-de-France Research Centre, Palaiseau, France
    For correspondence
    demian.wassermann@inria.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5194-6056

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.

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."

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.

Metrics

  • 998
    views
  • 191
    downloads
  • 13
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Majd Abdallah
  2. Gaston E Zanitti
  3. Valentin Iovene
  4. Demian Wassermann
(2022)
Functional gradients in the human lateral prefrontal cortex revealed by a comprehensive coordinate-based meta-analysis
eLife 11:e76926.
https://doi.org/10.7554/eLife.76926

Share this article

https://doi.org/10.7554/eLife.76926

Further reading

    1. Neuroscience
    Yafen Li, Yixuan Lin ... Antao Chen
    Research Article

    Concurrent verbal working memory task can eliminate the color-word Stroop effect. Previous research, based on specific and limited resources, suggested that the disappearance of the conflict effect was due to the memory information preempting the resources for distractors. However, it remains unclear which particular stage of Stroop conflict processing is influenced by working memory loads. In this study, electroencephalography (EEG) recordings with event-related potential (ERP) analyses, time-frequency analyses, multivariate pattern analyses (MVPAs), and representational similarity analyses (RSAs) were applied to provide an in-depth investigation of the aforementioned issue. Subjects were required to complete the single task (the classical manual color-word Stroop task) and the dual task (the Sternberg working memory task combined with the Stroop task), respectively. Behaviorally, the results indicated that the Stroop effect was eliminated in the dual-task condition. The EEG results showed that the concurrent working memory task did not modulate the P1, N450, and alpha bands. However, it modulated the sustained potential (SP), late theta (740–820 ms), and beta (920–1040 ms) power, showing no difference between congruent and incongruent trials in the dual-task condition but significant difference in the single-task condition. Importantly, the RSA results revealed that the neural activation pattern of the late theta was similar to the response interaction pattern. Together, these findings implied that the concurrent working memory task eliminated the Stroop effect through disrupting stimulus-response mapping.

    1. Neuroscience
    Samuel Noorman, Timo Stein ... Simon van Gaal
    Research Article

    This study investigates failures in conscious access resulting from either weak sensory input (perceptual impairments) or unattended input (attentional impairments). Participants viewed a Kanizsa stimulus with or without an illusory triangle within a rapid serial visual presentation of distractor stimuli. We designed a novel Kanizsa stimulus that contained additional ancillary features of different complexity (local contrast and collinearity) that were independently manipulated. Perceptual performance on the Kanizsa stimulus (presence vs. absence of an illusion) was equated between the perceptual (masking) and attentional (attentional blink) manipulation to circumvent common confounds related to conditional differences in task performance. We trained and tested classifiers on electroencephalogram (EEG) data to reflect the processing of specific stimulus features, with increasing levels of complexity. We show that late stages of processing (~200–250 ms), reflecting the integration of complex stimulus features (collinearity, illusory triangle), were impaired by masking but spared by the attentional blink. In contrast, decoding of local contrast (the spatial arrangement of stimulus features) was observed early in time (~80 ms) and was left largely unaffected by either manipulation. These results replicate previous work showing that feedforward processing is largely preserved under both perceptual and attentional impairments. Crucially, however, under matched levels of performance, only attentional impairments left the processing of more complex visual features relatively intact, likely related to spared lateral and local feedback processes during inattention. These findings reveal distinct neural mechanisms associated with perceptual and attentional impairments and thus contribute to a comprehensive understanding of distinct neural stages leading to conscious access.