Rapid acquisition of novel interface control by small ensembles of arbitrarily selected primary motor cortex neurons

J Neurophysiol. 2014 Sep 15;112(6):1528-48. doi: 10.1152/jn.00373.2013. Epub 2014 Jun 11.

Abstract

Pioneering studies demonstrated that novel degrees of freedom could be controlled individually by directly encoding the firing rate of single motor cortex neurons, without regard to each neuron's role in controlling movement of the native limb. In contrast, recent brain-computer interface work has emphasized decoding outputs from large ensembles that include substantially more neurons than the number of degrees of freedom being controlled. To bridge the gap between direct encoding by single neurons and decoding output from large ensembles, we studied monkeys controlling one degree of freedom by comodulating up to four arbitrarily selected motor cortex neurons. Performance typically exceeded random quite early in single sessions and then continued to improve to different degrees in different sessions. We therefore examined factors that might affect performance. Performance improved with larger ensembles. In contrast, other factors that might have reflected preexisting synaptic architecture-such as the similarity of preferred directions-had little if any effect on performance. Patterns of comodulation among ensemble neurons became more consistent across trials as performance improved over single sessions. Compared with the ensemble neurons, other simultaneously recorded neurons showed less modulation. Patterns of voluntarily comodulated firing among small numbers of arbitrarily selected primary motor cortex (M1) neurons thus can be found and improved rapidly, with little constraint based on the normal relationships of the individual neurons to native limb movement. This rapid flexibility in relationships among M1 neurons may in part underlie our ability to learn new movements and improve motor skill.

Keywords: brain-computer interface; comodulation; neural trajectory; neuron ensemble; null space.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain-Computer Interfaces
  • Macaca mulatta
  • Male
  • Motor Cortex / cytology
  • Motor Cortex / physiology*
  • Motor Skills*
  • Neurons / physiology*
  • Synapses / physiology*