Reward Modulates Local Field Potentials, Spiking Activity and Spike-Field Coherence in the Primary Motor Cortex

Abstract

Number of words (Abstract): Number of words (Significance Statement): Number of words (Introduction): Number of words (Discussion):Conflict of Interest: The authors declare no conflict of interests. ABSTRACTReward modulation of the primary motor cortex (M1) could be exploited in developing an autonomously updating brain-machine interface (BMI) based on a reinforcement learning architecture. In order to understand the multifaceted effects of reward on M1 activity, we investigated how neural spiking, oscillatory activities and their functional interactions are modulated by conditioned stimuli related reward expectation. To do so, local field potentials (LFPs) and singleunit/multi-unit activities were recorded simultaneously and bilaterally from M1 cortices while five non-human primates performed cued center-out reaching or grip force tasks either manually using their right arm/hand or observed passively.We found that reward expectation influenced the strength of alpha (8)(9)(10)(11)(12)(13)(14) power, alpha-gamma comodulation, alpha spike-field coherence, and firing rates in general in M1. Furthermore, we found that an increase in alpha-band power was correlated with a decrease in neural spiking activity, that firing rates were highest at the trough of the alpha-band cycle and lowest at the peak of its cycle.These findings imply that alpha oscillations modulated by reward expectation have an influence on spike firing rate and spike timing during both reaching and grasping tasks in M1. These LFP, spike, and spike-field interactions could be used to follow the M1 neural state in order to enhance BMI decoding Zhao et al., 2018). Significance StatementKnowing the subjective value of performed or observed actions is valuable feedback that can be used to improve the performance of an autonomously updating brain-machine interface (BMI). Reward-related information in the primary motor cortex (M1) may be crucial for more stable and robust BMI decoding (Zhao et al., 2018). Here, we present how expectation of reward during motor tasks, or simple observation, is represented by increased spike firing rates in conjunction with decreased alpha (8-14 Hz) oscillatory power, alpha-gamma comodulation, and alpha spike-field coherence, as compared to non-rewarding trials. Moreover, a phasic relation between alpha oscillations and firing rates was observed where firing rates were found to be lowest and highest at the peak and trough of alpha oscillations, respectively.

A Brain to Spine Interface for Transferring Artificial Sensory Information

“…This latter finding is similar to our previous observation that M1, S1 and dorsal premotor (pMd) neurons in primates increase their firing rates when the animal's reward expectation is not met 54,55 . A recent study showed that M1 LFP spectral power in the 8-14 Hz band increased in non-rewarding trials as compared to rewarded trials in a primate center-out reaching task 56 . This is consistent with the increase in spectral power observed in our study when encoder rats didn't receive a feedback reward in our study.…”

Motor Cortex Encodes A Temporal Difference Reinforcement Learning Process

“…We recently showed that this reward modulation of directional tuning holds during intracortical brain computer interface control (iBCI) when utilizing M1 (23), and that M1 grip force tuning functions are modulated by reward during manual control (23). In addition, we have recently discovered that reward modulation influences the relationship in M1 between the local field and individual neurons, where the spike field coherence is upregulated during nonrewarding trials as is the phase amplitude coupling between alpha phase and gamma amplitude (24).…”

A Brain to Spine Interface for Transferring Artificial Sensory Information

“…Incidentally, M1, S1 and dorsal premotor (pMd) neurons in primates increase their firing rates when reward expectation is not met 54,55 . A recent study showed that M1 LFP spectral power in the 8-14 Hz band increased in non-rewarding trials as compared to rewarded trials in a primate center-out reaching task 56 . This is consistent with the increase in spectral power observed when encoder rats didn't receive a feedback reward in our study.…”