Frontal network dynamics reflect neurocomputational mechanisms for reducing maladaptive biases in motivated action

PLoS Biol. 2018 Oct 18;16(10):e2005979. doi: 10.1371/journal.pbio.2005979. eCollection 2018 Oct.

Abstract

Motivation exerts control over behavior by eliciting Pavlovian responses, which can either match or conflict with instrumental action. We can overcome maladaptive motivational influences putatively through frontal cognitive control. However, the neurocomputational mechanisms subserving this control are unclear; does control entail up-regulating instrumental systems, down-regulating Pavlovian systems, or both? We combined electroencephalography (EEG) recordings with a motivational Go/NoGo learning task (N = 34), in which multiple Go options enabled us to disentangle selective action learning from nonselective Pavlovian responses. Midfrontal theta-band (4 Hz-8 Hz) activity covaried with the level of Pavlovian conflict and was associated with reduced Pavlovian biases rather than reduced instrumental learning biases. Motor and lateral prefrontal regions synchronized to the midfrontal cortex, and these network dynamics predicted the reduction of Pavlovian biases over and above local, midfrontal theta activity. This work links midfrontal processing to detecting Pavlovian conflict and highlights the importance of network processing in reducing the impact of maladaptive, Pavlovian biases.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Bias
  • Choice Behavior / physiology
  • Computer Simulation
  • Conditioning, Operant / physiology*
  • Decision Making / physiology
  • Electroencephalography / methods
  • Female
  • Frontal Lobe / physiology*
  • Humans
  • Learning / physiology
  • Male
  • Motivation / physiology*
  • Theta Rhythm

Grants and funding

Netherlands Organization for Scientific Research (NWO) www.nwo.nl (grant number 406-14-028). Received by JCS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The National Science Foundation www.nsf.gov (grant number 1460604). Received by MJF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Institute for Mental Health www.nimh.nih.gov (grant number MH080066-01). Received by MJF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Netherlands Organization for Scientific Research (NWO) www.nwo.nl (grant number 453-14-005). Received by RC. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. James S. McDonnell Foundation www.jsmf.org. Received by RC. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Netherlands Organization for Scientific Research (NWO) www.nwo.nl (grant number 451-11-004). Received by HEMdO. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. James S. McDonnell Foundation Understanding Human Cognition Collaborative Award (grant number 220020448). Received by OJ. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Wellcome Trust Investigator Award in Science (grant number 207550). Received by OJ. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Royal Society Wolfson Research Merit Award. Received by OJ. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.