Effective Connectivity Reveals Important Roles for Both the Hyperdirect (Fronto-Subthalamic) and the Indirect (Fronto-Striatal-Pallidal) Fronto-Basal Ganglia Pathways during Response Inhibition
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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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In demanding situations of action conflict, the basal ganglia keep all responses in check until further processing has converged on an action decision, and the final call is received from the pre-SMA and other prefrontal regions.
“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
The Introduction and Discussion (pages unavailable in our copy) link pre-SMA and other frontal regions to basal-ganglia pathways involved in response inhibition, and describe successful stopping as having downstream inhibitory effects on motor cortex. They do not establish that the basal ganglia hold all responses in check until a decision has converged and a final call arrives from prefrontal regions. (LLM, conf=0.84)
Experimental — accuracy not yet measuredFrontostriatal circuits capitalizing on inferior frontal cortex, pre-SMA, and basal ganglia are engaged when impulsive actions are to be interrupted, aborted, suppressed, or overridden by more appropriate actions, even when action control is triggered unconsciously.
“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
In demanding situations of action conflict, the inferior frontal cortex is recruited to aid in implementing response inhibition.
“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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Self-citation
- 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 › Neurology › Neurological disorders and treatments
- 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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