Roles of the prefrontal cortex in learning to time the onset of pre-existing motor programs

PLoS One. 2020 Nov 9;15(11):e0241562. doi: 10.1371/journal.pone.0241562. eCollection 2020.

Abstract

The prefrontal cortex (PFC) is involved in cognitive control of motor activities and timing of future intensions. This study investigated the cognitive control of balance recovery in response to unpredictable gait perturbations and the role of PFC subregions in learning by repetition. Bilateral dorsolateral (DLPFC), ventrolateral (VLPFC), frontopolar (FPFC) and orbitofrontal (OFC) cortex hemodynamic changes induced by unpredictable slips were analyzed as a function of successive trials in ten healthy young adults. Slips were induced by the acceleration of one belt as the participant walked on a split-belt treadmill. A portable functional near-infrared spectroscope monitored PFC activities quantified by oxyhemoglobin (ΔO2Hb) and deoxyhemoglobin (ΔHbR) during the consecutive trial phases: standing, walking, slip-recovery. During the first 3 trials, the average oxyhemoglobin (ΔO2Hbavg) in the DLPFC, VLPFC, FPFC, and OFC cortex was significantly higher during slip-recovery than unperturbed walking or the standing baseline. Then, ΔO2Hbavg decreased progressively from trial-to-trial in the DLPFC, VLPFC, and FPFC, but increased and then remained constant in the OFC. The average deoxyhemoglobin (ΔHbRavg) presented mirror patterns. These changes after the third trial were paralleled by the progressive improvement of recovery revealed by kinematic variables. The results corroborate our previous hypothesis that only timing of the onset of a "good enough recovery motor program" is learned with practice. They also strongly support the assumption that the PFC contributes to the recall of pre-existing motor programs whose onset timing is adjusted by the OFC. Hence, learning is clearly divided into two steps delineated by the switch in activity of the OFC. Additionally, motor processes appear to share the working memory as well as decisional and predictive resources of the cognitive system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain Mapping
  • Female
  • Gait / physiology*
  • Healthy Volunteers
  • Hemoglobins / analysis
  • Hemoglobins / metabolism
  • Humans
  • Learning / physiology*
  • Male
  • Oxyhemoglobins / analysis
  • Oxyhemoglobins / metabolism
  • Postural Balance / physiology*
  • Prefrontal Cortex / blood supply
  • Prefrontal Cortex / physiology*
  • Spectroscopy, Near-Infrared
  • Young Adult

Substances

  • Hemoglobins
  • Oxyhemoglobins
  • deoxyhemoglobin

Grants and funding

BCL received the following funding. This work was supported by the Ministry of Science, ICT and Future Planning south Korea/Institute for Information and Communications Technology Promotion (IITP): # 2017-0-01724. The funding agency provided support in the form of salaries for author BCL, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section