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Articles, Behavioral/Cognitive

Frequency-Dependent Representation of Reinforcement-Related Information in the Human Medial and Lateral Prefrontal Cortex

Elliot H. Smith, Garrett P. Banks, Charles B. Mikell, Syndey S. Cash, Shaun R. Patel, Emad N. Eskandar and Sameer A. Sheth
Journal of Neuroscience 2 December 2015, 35 (48) 15827-15836; DOI: https://doi.org/10.1523/JNEUROSCI.1864-15.2015
Elliot H. Smith
1Department of Neurological Surgery, Columbia University Medical Center, New York, New York 10032, and
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Garrett P. Banks
1Department of Neurological Surgery, Columbia University Medical Center, New York, New York 10032, and
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Charles B. Mikell
1Department of Neurological Surgery, Columbia University Medical Center, New York, New York 10032, and
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Syndey S. Cash
2Departments of Neurology and
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Shaun R. Patel
3Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114
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Emad N. Eskandar
3Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114
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Sameer A. Sheth
1Department of Neurological Surgery, Columbia University Medical Center, New York, New York 10032, and
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Abstract

The feedback-related negativity (FRN) is a commonly observed potential in scalp electroencephalography (EEG) studies related to the valence of feedback about a subject's performance. This potential classically manifests as a negative deflection in medial frontocentral EEG contacts following negative feedback. Recent work has shown prominence of theta power in the spectral composition of the FRN, placing it within the larger class of “frontal midline theta” cognitive control signals. Although the dorsal anterior cingulate cortex (dACC) is thought to be the cortical generator of the FRN, conclusive data regarding its origin and propagation are lacking. Here we examine intracranial electrophysiology from the human medial and lateral prefrontal cortex (PFC) to better understand the anatomical localization and communication patterns of the FRN. We show that the FRN is evident in both low- and high-frequency local field potentials (LFPs) recorded on electrocorticography. The FRN is larger in medial compared with lateral PFC, and coupling between theta band phase and high-frequency LFP power is also greater in medial PFC. Using Granger causality and conditional mutual information analyses, we provide evidence that feedback-related information propagates from medial to lateral PFC, and that this information transfer oscillates with theta-range periodicity. These results provide evidence for the dACC as the cortical source of the FRN, provide insight into the local computation of frontal midline theta, and have implications for reinforcement learning models of cognitive control.

SIGNIFICANCE STATEMENT Using intracranial electrophysiology in humans, this work addresses questions about a frequently studied feedback-related electroencephalographic signal, illuminating anatomical and functional properties of the representation of feedback-related reinforcement during decision-making across the medial to lateral extent of the human prefrontal cortex.

  • electrocorticography
  • feedback-related negativity
  • frontal midline theta
  • information representation
  • prefrontal cortex
  • reinforcement
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The Journal of Neuroscience: 35 (48)
Journal of Neuroscience
Vol. 35, Issue 48
2 Dec 2015
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Frequency-Dependent Representation of Reinforcement-Related Information in the Human Medial and Lateral Prefrontal Cortex
Elliot H. Smith, Garrett P. Banks, Charles B. Mikell, Syndey S. Cash, Shaun R. Patel, Emad N. Eskandar, Sameer A. Sheth
Journal of Neuroscience 2 December 2015, 35 (48) 15827-15836; DOI: 10.1523/JNEUROSCI.1864-15.2015

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Frequency-Dependent Representation of Reinforcement-Related Information in the Human Medial and Lateral Prefrontal Cortex
Elliot H. Smith, Garrett P. Banks, Charles B. Mikell, Syndey S. Cash, Shaun R. Patel, Emad N. Eskandar, Sameer A. Sheth
Journal of Neuroscience 2 December 2015, 35 (48) 15827-15836; DOI: 10.1523/JNEUROSCI.1864-15.2015
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Keywords

  • electrocorticography
  • feedback-related negativity
  • frontal midline theta
  • information representation
  • prefrontal cortex
  • reinforcement

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