Cortical neurons multiplex reward-related signals along with sensory and motor information

Abstract

Rewards are known to influence neural activity associated with both motor preparation and execution. This influence can be exerted directly upon the primary motor (M1) and somatosensory (S1) cortical areas via the projections from reward-sensitive dopaminergic neurons of the midbrain ventral tegmental areas. However, the neurophysiological manifestation of reward-related signals in M1 and S1 are not well understood. Particularly, it is unclear how the neurons in these cortical areas multiplex their traditional functions related to the control of spatial and temporal characteristics of movements with the representation of rewards. To clarify this issue, we trained rhesus monkeys to perform a center-out task in which arm movement direction, reward timing, and magnitude were manipulated independently. Activity of several hundred cortical neurons was simultaneously recorded using chronically implanted microelectrode arrays. Many neurons (9-27%) in both M1 and S1 exhibited activity related to reward anticipation. Additionally, neurons in these areas responded to a mismatch between the reward amount given to the monkeys and the amount they expected: A lower-than-expected reward caused a transient increase in firing rate in 60-80% of the total neuronal sample, whereas a larger-than-expected reward resulted in a decreased firing rate in 20-35% of the neurons. Moreover, responses of M1 and S1 neurons to reward omission depended on the direction of movements that led to those rewards. These observations suggest that sensorimotor cortical neurons corepresent rewards and movement-related activity, presumably to enable reward-based learning.

Motor Cortex Encodes A Temporal Difference Reinforcement Learning Process

“…Multiple units in M1 have been shown to respond to the conditioned (CS) and unconditioned stimuli (US) (2,(15)(16)(17). We have also reported previously (2) and in Fig.3 that the average activity of M1 is significantly different throughout a rewarding trial with respect to a nonrewarding trial.…”

“…Previously we, and others, have shown that reward modulates single units and local field potentials in the primary sensorimotor cortices (M1, S1) of non-human primates (2,(15)(16)(17) and frontal regions influencing M1 (18). We have proposed that neural correlates of reward could be used towards an autonomously updating brain machine interface (2,17).…”

“…M1 acquires a response to a conditioned stimulus (CS) following conditioning when the CS is used to cue reward. Reward prediction error, an important aspect of the TDRL process, is also encoded in M1 (15) and after an unexpected reward omission. If reward is temporally predictable, then M1 tracks the underlying temporal structure as well.…”

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 .…”

Neuronal activity in the premotor cortex of monkeys reflects both cue salience and motivation for action generation and inhibition

“…Electrophysiological, imaging and lesion studies succeeded in identifying motivation-related and rewardrelated signals in different brain areas [1][2][3] . While prefrontal and parietal cortex seem more involved in encoding the value and salience of the sensory signals used to inform about the incoming reward, the activity in motor cortical areas was proposed to be mostly related to the motivation to perform an action 4,5 even if modulated by other factors like reward expectation 6,7 , reward feedback 8 , and anticipation of reward delivery 9 .…”