Simultaneous Multiplexing of Movement Execution, Observation, and Reward in Cortical Motor Neurons

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2021

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Abstract

Neural activities of the motor cortices have been traditionally known to represent motor information such as velocity of the movement and muscle force. Recent studies show that motor cortices, including primary motor cortex (M1), also represent non-traditional information such as observed movements of others and reward-related signal. However, how the neurons simultaneously multiplex such non-traditional information along with traditional motor parameters and whether the multiplexing leads to significant interactions are not well understood. Furthermore, understanding how the non-traditional information are encoded and they interact with motor information may help the development of more error-resistant, autonomous brain-to-machine interface and the understanding of underlying mechanism behind joint action and motor skill learning. In this dissertation, we investigate in detail how the observed movements and reward are simultaneously multiplexed along with traditional motor information and how each pair of neural representations interact with each other. First, regarding movement observation, we show that significant fraction of M1 neurons simultaneously encode the presence and direction of the movement of others along with those of self-movements. Neurons respond differently to joint action than to self-movements and show an interaction effect from the two representations of observed and executed movements rather than simple averaging of the two. Some neurons that separately encode observed and executed movements turn to suppress the representation of observed movements in joint action. In simultaneous actions, the representation of self-executed movement gets weaker, which suggests an interaction between two information and may possibly lead to behavioral interference. Preferred directions also change to be decoupled for noncongruent joint actions as to allow simultaneous multiplexing of both information with phase difference, while being synced for congruent ones. Conditional probabilities from the distribution of encoding neurons suggest a shared circuitry for movement observation, execution, and simultaneous actions. Shared circuitry with interactions between representations may explain why people can perform movements freely while watching others move; yet if the interaction between the two goes up due to simultaneous occurrence, it may result in interferences in behavior. Second, regarding the multiplexing of reward-related signal with movement signals, we show that both signals are multiplexed in individual and population neurons in M1 and S1. The activity of neural population in M1 and S1 distinguished whether the reward timing before the delivery of the reward. Furthermore, reward per se, reward anticipation, and reward prediction error (RPE) were encoded along with the motor information. The encoding of the reward-related signal interacted with the motor information in that the preferred direction changed when the reward was omitted. Change of spatial tuning of neurons due to reward prediction error signifies that there is interaction between the neural representation of reward and motor information, which may impact and underlie motor skill learning. In conclusion, both observed movements and reward are simultaneously multiplexed with traditional motor information. Co-representation of the two non-traditional information then leads to interaction between them and the motor information. Such interaction suggest that such simultaneous multiplexing may lead to behavioral interferences and motor skill learning.

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Byun, Yoon Woo (2021). Simultaneous Multiplexing of Movement Execution, Observation, and Reward in Cortical Motor Neurons. Dissertation, Duke University. Retrieved from https://hdl.handle.net/10161/24365.

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