Dynamics of single neuron activity in monkey primary motor cortex related to sensorimotor transformation

Abstract

We investigated the dynamics of neuronal activity related to sensorimotor transformation during single experimental trials of a given stimulus-response (S-R) association task. A monkey was trained to perform wrist extension/flexion movements in the horizontal plane to align a pointer with a visual target while single unit activity in the primary motor cortex (MI) was being recorded. The stimulus was a colored light-emitting diode (LED) presented to either the left or right of a central reference point. The monkey had to point directly at the target ('compatible' S-R mapping) or point to the opposite side of the target position ('incompatible' S-R mapping), with the mapping rule specified by the color of the LED. Single neuron activities on the four correct trials (left/right stimulus x compatible/incompatible S-R mapping) were compared to determine whether such activities were more related to stimulus encoding and representation, to response preparation and execution, or to the 'decision' processes translating the stimulus representation into a response representation. A novel mathematical technique, called LOCUS ANALYSIS, has been developed to quantitatively analyze and visualize the contribution of neuronal activity toward the sensory, motor, or sensorimotor (i.e., decisional) aspects of the task. Our data show that as a thai evolves, neuronal activity in MI, at a population level, is first correlated with the representation of the specific stimulus (the side of LED), then with the representation of the S-R mapping rule (the color of LED) as well as trial-specific S-R association (the conjunction of stimulus side and stimulus color), and finally with the representation of the behavioral response (extension or flexion wrist movement). Immediately after the issuance of the movement command, the populational activity in MI remains correlated with the trial-specific stimulus-response conjunctions, i.e., the context of the motor decision that the monkey has just made. Cells recorded successively in a single penetration tend to resemble each other in their pattern of firing on the four correct trials, suggesting a modular organization of neurons based on their functional role in the processing of the S-R association task. Our results indicate that MI belongs to a distributed network such that its neuronal activity reflects the underlying network dynamics that translate a stimulus representation into a response representation via the activation and application of appropriate S-R mapping rule.