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Effective Connectivity Reveals Important Roles for Both the Hyperdirect (Fronto-Subthalamic) and the Indirect (Fronto-Striatal-Pallidal) Fronto-Basal Ganglia Pathways during Response Inhibition
Open accessAbstract
Fronto-basal ganglia pathways play a crucial role in voluntary action control, including the ability to inhibit motor responses. Response inhibition might be mediated via a fast hyperdirect pathway connecting the right inferior frontal gyrus (rIFG) and the presupplementary motor area (preSMA) with the subthalamic nucleus or, alternatively, via the indirect pathway between the cortex and caudate. To test the relative contribution of these two pathways to inhibitory action control, we applied an innovative quantification method for effective brain connectivity. Functional magnetic resonance imaging data were collected from 20 human participants performing a Simon interference task with an occasional stop signal. A single right-lateralized model involving both the hyperdirect and indirect pathways best explained the pattern of brain activation on stop trials. Notably, the overall connection strength of this combined model was highest on successfully inhibited trials. Inspection of the relationship between behavior and connection values revealed that fast inhibitors showed increased connectivity between rIFG and right caudate (rCaudate), whereas slow inhibitors were associated with increased connectivity between preSMA and rCaudate. In compliance, connection strengths from the rIFG and preSMA into the rCaudate were correlated negatively. If participants failed to stop, the magnitude of experienced interference (Simon effect), but not stopping latency, was predictive for the hyperdirect–indirect model connections. Together, the present results suggest that both the hyperdirect and indirect pathways act together to implement response inhibition, whereas the relationship between performance control and the fronto-basal ganglia connections points toward a top-down mechanism that underlies voluntary action control.
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“and the basal ganglia keep all responses in check until further processing has converged on an action decision, and the final call is received from upstream: from the pre-SMA and other prefrontal regions (Jahfari et al., 2011).”
From Impulsive action: emotional impulses and their control (2014) · cites this paper as Jahfari et al., 2011
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“Frontostriatal circuits in the brain, capitalizing on the inferior frontal cortex, the pre-supplementary motor area (pre-SMA), and the basal ganglia, are engaged when impulsive actions are to be interrupted, aborted, suppressed, or overridden by more appropriate actions (Jahfari et al., 2011; Ridderinkhof et al., 2011), even when such action control is triggered unconsciously (van Gaal et al., 200”
From Impulsive action: emotional impulses and their control (2014) · cites this paper as Jahfari et al., 2011
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“the inferior frontal cortex is recruited to aid in implementing response inhibition (Jahfari et al., 2011; Swann et al., 2012)”
From Impulsive action: emotional impulses and their control (2014) · cites this paper as Jahfari et al., 2011
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Mendes, A. J., Galdo‐Álvarez, S., Lema, A., Carvalho, S., & Leite, J. (2022) · Research Square · doi:10.21203/rs.3.rs-1453687/v1
An fMRI study of inflectional encoding in spoken word production: Role of domain-general inhibition
Ferreira, J., Roelofs, A., Freches, G. B., & Piai, V. (2023) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2023.108653
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Ascenzi, B. M., Caldas, G. D. C., Frati, A., Santoro, A., & Palmieri, M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-822404-5.00021-8
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Weichart, E. R., Francis, C., & Sederberg, P. B. (2024) · doi:10.31234/osf.io/fqg7e
Szabó, J. P., Hegedüs, P., Laszlovszky, T., Halász, L., Miklós, G., Király, B., Perczel, G., Bokodi, V., Entz, L., Ulbert, I., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-71502-z
Wild, A., Tziraki, M., Lea‐Carnall, C., & Garg, S. (2025) · medRxiv · doi:10.1101/2025.01.27.25321195
Robertazzi, F., Vissani, M., & Falotico, E. (2025) · International Journal of Neural Systems · doi:10.1142/s0129065725500406
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Fang, Z., Sack, A. T., & Leunissen, I. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.25.690566
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Metadata
- Authors
- Jahfari, S., Waldorp, L., van den Wildenberg, W. P. M., Scholte, H. S., Ridderinkhof, K. R., & Forstmann, B. U.
- Affiliations
- University of Amsterdam (NL)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-05-04
- Volume
- 31
- Issue
- 18
- Pages
- 6891-6899
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6632844
- OpenAlex
- W2100219975
- Cited by
- 308
- References
- 44
- Citations by year
- 2026: 11 · 2025: 15 · 2024: 19 · 2023: 5 · 2022: 21 · 2021: 27 · 2020: 17 · 2019: 18 · 2018: 26 · 2017: 17 · 2016: 20 · 2015: 30 · 2014: 29 · 2013: 29 · 2012: 20
- FWCI
- 13.14
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- response inhibition, hyperdirect pathway, indirect pathway, effective connectivity, subthalamic nucleus, caudate nucleus, inferior frontal gyrus, pre-supplementary motor area, stop signal, top-down control
- MeSH terms
- Adolescent, Adult, Analysis of Variance, Brain Mapping, Corpus Striatum, Female, Frontal Lobe, Globus Pallidus, Humans, Image Processing, Computer-Assisted, Inhibition, Psychological, Magnetic Resonance Imaging, Male, Neural Pathways, Neuropsychological Tests, Reaction Time, Subthalamic Nucleus
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