Neural population variance explains adaptation differences during learning

Abstract

Variability, a ubiquitous feature of neural activity, plays an integral role in behavior. However, establishing a causal relationship between neural signals and behavior is difficult. By defining a mathematical mapping between neural spiking activity and behavior, we investigate the role of spiking variability in adaptation during a brain-computer interface (BCI) behavior in male rhesus macaques (Macaca mulatta, n=2). Recent BCI evidence demonstrates that creating novel neural patterns is harder than repurposing existing patterns to respond to changes in external input. However, what limits the ability to repurpose, or adapt, patterns under different magnitudes of change is less well-characterized. Here, we present evidence that variance in neural spiking activity reveals differences in learnability between easy and hard adaptation conditions and across sessions. Furthermore, our study illuminates the limitations in neural changes underlying behavior within a neurofeedback paradigm. Significance StatementVariability in neural activity is a major driver of behavioral variability, though it is unclear how variability is balanced with stable neural activity as new behaviors become more practiced. By using a brain-computer interface methodology, we define a mathematical mapping between neural spiking activity and a behavioral control signal. Through thoughtful manipulation of this mapping, we incite the subjects (rhesus macaques) to learn and adapt neural activity to regain behavioral proficiency. We find that metrics of neural population variability are differentially modulated depending on difficulty of the imposed manipulation. Our exciting results provide important implications for brain-computer interface applications as well as our understanding of learning and adaptation more broadly. Our work represents an important step forwards towards understanding population neural dynamics in this critical component of behavior.