A Cognition-Related Neural Oscillation Pattern, Generated in the Prelimbic Cortex, Can Control Operant Learning in Rats

J Neurosci. 2017 Jun 14;37(24):5923-5935. doi: 10.1523/JNEUROSCI.3651-16.2017. Epub 2017 May 23.

Abstract

The prelimbic (PrL) cortex constitutes one of the highest levels of cortical hierarchy dedicated to the execution of adaptive behaviors. We have identified a specific local field potential (LFP) pattern generated in the PrL cortex and associated with cognition-related behaviors. We used this pattern to trigger the activation of a visual display on a touch screen as part of an operant conditioning task. Rats learned to increase the presentation rate of the selected θ to β-γ (θ/β-γ) transition pattern across training sessions. The selected LFP pattern appeared to coincide with a significant decrease in the firing of PrL pyramidal neurons and did not seem to propagate to other cortical or subcortical areas. An indication of the PrL cortex's cognitive nature is that the experimental disruption of this θ/β-γ transition pattern prevented the proper performance of the acquired task without affecting the generation of other motor responses. The use of this LFP pattern to trigger an operant task evoked only minor changes in its electrophysiological properties. Thus, the PrL cortex has the capability of generating an oscillatory pattern for dealing with environmental constraints. In addition, the selected θ/β-γ transition pattern could be a useful tool to activate the presentation of external cues or to modify the current circumstances.SIGNIFICANCE STATEMENT Brain-machine interfaces represent a solution for physically impaired people to communicate with external devices. We have identified a specific local field potential pattern generated in the prelimbic cortex and associated with goal-directed behaviors. We used the pattern to trigger the activation of a visual display on a touch screen as part of an operant conditioning task. Rats learned to increase the presentation rate of the selected field potential pattern across training. The selected pattern was not modified when used to activate the touch screen. Electrical stimulation of the recording site prevented the proper performance of the task. Our findings show that the prelimbic cortex can generate oscillatory patterns that rats can use to control their environment for achieving specific goals.

Keywords: behaving rats; brain–machine interaction; local field potentials; neural oscillations; operant conditioning; prelimbic cortex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Clocks / physiology*
  • Brain Waves / physiology
  • Brain-Computer Interfaces*
  • Cognition / physiology*
  • Conditioning, Operant / physiology*
  • Evoked Potentials / physiology
  • Feedback, Physiological / physiology
  • Limbic Lobe / physiology*
  • Male
  • Nerve Net / physiology*
  • Rats