Audio-induced medial prefrontal cortical dynamics enhances coadaptive learning in brain–machine interfaces

Abstract

Abstract Objectives. Coadaptive brain–machine interfaces (BMIs) allow subjects and external devices to adapt to each other during the closed-loop control, which provides a promising solution for paralyzed individuals. Previous studies have focused on either improving sensory feedback to facilitate subject learning or developing adaptive algorithms to maintain stable decoder performance. In this work, we aim to design an efficient coadaptive BMI framework which not only facilitates the learning of subjects on new tasks with designed sensory feedback, but also improves decoders’ learning ability by extracting sensory feedback-induced evaluation information. Approach. We designed dynamic audio feedback during the trial according to the subjects’ performance when they were trained to learn a new behavioral task. We compared the learning performance of two groups of Sprague Dawley rats, one with and the other without the designed audio feedback to show whether this audio feedback could facilitate the subjects’ learning. Compared with the traditional closed-loop in BMI systems, an additional closed-loop involving medial prefrontal cortex (mPFC) activity was introduced into the coadaptive framework. The neural dynamics of audio-induced mPFC activity was analyzed to investigate whether a significant neural response could be triggered. This audio-induced response was then translated into reward expectation information to guide the learning of decoders on a new task. The multiday decoding performance of the decoders with and without audio-induced reward expectation was compared to investigate whether the extracted information could accelerate decoders to learn a new task. Main results. The behavior performance comparison showed that the average days for rats to achieve 80% well-trained behavioral performance was improved by 26.4% after introducing the designed audio feedback sequence. The analysis of neural dynamics showed that a significant neural response of mPFC activity could be elicited by the audio feedback and the visualization of audio-induced neural patterns was emerged and accompanied by the behavioral improvement of subjects. The multiday decoding performance comparison showed that the decoder taking the reward expectation information could achieve faster task learning by 33.8% on average across subjects. Significance. This study demonstrates that the designed audio feedback could improve the learning of subjects and the mPFC activity induced by audio feedback can be utilized to improve the decoder’s learning efficiency on new tasks. The coadaptive framework involving mPFC dynamics in the closed-loop interaction can advance the BMIs into a more adaptive and efficient system with learning ability on new tasks.