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Causal evidence for learning-dependent frontal lobe contributions to cognitive control

(2018) JOURNAL OF NEUROSCIENCE. 38(4). p.962-973
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Abstract
The lateral prefrontal cortex (LPFC) plays a central role in the prioritization of sensory input based on task relevance. Such top-down control of perception is of fundamental importance in goal-directed behavior, but can also be costly when deployed excessively, necessitating a mechanism that regulates control engagement to align it with changing environmental demands. We have recently introduced the "flexible control model" (FCM), which explains this regulation as resulting from a self-adjusting reinforcement-learning mechanism that infers latent statistical structure in dynamic task environments to predict forthcoming states. From this perspective, LPFC-based control is engaged as a function of anticipated cognitive demand, a notion for which we previously obtained correlative neuroimaging evidence. Here, we put this hypothesis to a rigorous, causal test by combining the FCM with a transcranial magnetic stimulation (TMS) intervention that transiently perturbed the LPFC. Human participants (male and female) completed a nonstationary version of the Stroop task with dynamically changing probabilities of conflict between task-relevant and task-irrelevant stimulus features. TMS was given on each trial before stimulus onset either over the LPFC or over a control site. In the control condition, we observed adaptive performance fluctuations consistent with demand predictions that were inferred from recent and remote trial history and effectively captured by our model. Critically, TMS over the LPFC eliminated these fluctuations while leaving basic cognitive and motor functions intact. These results provide causal evidence for a learning-based account of cognitive control and delineate the nature of the signals that regulate top-down biases over stimulus processing.
Keywords
TRANSCRANIAL MAGNETIC STIMULATION, ANTERIOR CINGULATE CORTEX, TOP-DOWN, MODULATION, PREFRONTAL CORTEX, NEURAL MECHANISMS, INTEGRATIVE THEORY, EXECUTIVE CONTROL, WORKING-MEMORY, CONFLICT, ATTENTION, cognitive control, computational modeling, prefrontal cortex, reinforcement learning, transcranial magnetic stimulation

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Citation

Please use this url to cite or link to this publication:

Chicago
Muhle-Karbe, Paul Simon, Jiefeng Jiang, and Tobias Egner. 2018. “Causal Evidence for Learning-dependent Frontal Lobe Contributions to Cognitive Control.” Journal of Neuroscience 38 (4): 962–973.
APA
Muhle-Karbe, P. S., Jiang, J., & Egner, T. (2018). Causal evidence for learning-dependent frontal lobe contributions to cognitive control. JOURNAL OF NEUROSCIENCE, 38(4), 962–973.
Vancouver
1.
Muhle-Karbe PS, Jiang J, Egner T. Causal evidence for learning-dependent frontal lobe contributions to cognitive control. JOURNAL OF NEUROSCIENCE. Washington: Soc Neuroscience; 2018;38(4):962–73.
MLA
Muhle-Karbe, Paul Simon, Jiefeng Jiang, and Tobias Egner. “Causal Evidence for Learning-dependent Frontal Lobe Contributions to Cognitive Control.” JOURNAL OF NEUROSCIENCE 38.4 (2018): 962–973. Print.
@article{8608071,
  abstract     = {The lateral prefrontal cortex (LPFC) plays a central role in the prioritization of sensory input based on task relevance. Such top-down control of perception is of fundamental importance in goal-directed behavior, but can also be costly when deployed excessively, necessitating a mechanism that regulates control engagement to align it with changing environmental demands. We have recently introduced the "flexible control model" (FCM), which explains this regulation as resulting from a self-adjusting reinforcement-learning mechanism that infers latent statistical structure in dynamic task environments to predict forthcoming states. From this perspective, LPFC-based control is engaged as a function of anticipated cognitive demand, a notion for which we previously obtained correlative neuroimaging evidence. Here, we put this hypothesis to a rigorous, causal test by combining the FCM with a transcranial magnetic stimulation (TMS) intervention that transiently perturbed the LPFC. Human participants (male and female) completed a nonstationary version of the Stroop task with dynamically changing probabilities of conflict between task-relevant and task-irrelevant stimulus features. TMS was given on each trial before stimulus onset either over the LPFC or over a control site. In the control condition, we observed adaptive performance fluctuations consistent with demand predictions that were inferred from recent and remote trial history and effectively captured by our model. Critically, TMS over the LPFC eliminated these fluctuations while leaving basic cognitive and motor functions intact. These results provide causal evidence for a learning-based account of cognitive control and delineate the nature of the signals that regulate top-down biases over stimulus processing.},
  author       = {Muhle-Karbe, Paul Simon and Jiang, Jiefeng and Egner, Tobias},
  issn         = {0270-6474},
  journal      = {JOURNAL OF NEUROSCIENCE},
  keywords     = {TRANSCRANIAL MAGNETIC STIMULATION,ANTERIOR CINGULATE CORTEX,TOP-DOWN,MODULATION,PREFRONTAL CORTEX,NEURAL MECHANISMS,INTEGRATIVE THEORY,EXECUTIVE CONTROL,WORKING-MEMORY,CONFLICT,ATTENTION,cognitive control,computational modeling,prefrontal cortex,reinforcement learning,transcranial magnetic stimulation},
  language     = {eng},
  number       = {4},
  pages        = {962--973},
  publisher    = {Soc Neuroscience},
  title        = {Causal evidence for learning-dependent frontal lobe contributions to cognitive control},
  url          = {http://dx.doi.org/10.1523/JNEUROSCI.1467-17.2017},
  volume       = {38},
  year         = {2018},
}

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