Abstract
For years, neurophysiological studies of the cerebral cortical mechanisms of voluntary motor control were limited to single-electrode recordings of the activity of one or a few neurons at a time. This approach was supported by the widely accepted belief that single neurons were the fundamental computational units of the brain (the “neuron doctrine”). Experiments were guided by motor-control models that proposed that the motor system attempted to plan and control specific parameters of a desired action, such as the direction, speed or causal forces of a reaching movement in specific coordinate frameworks, and that assumed that the controlled parameters would be expressed in the task-related activity of single neurons. The advent of chronically implanted multi-electrode arrays about 20 years ago permitted the simultaneous recording of the activity of many neurons. This greatly enhanced the ability to study neural control mechanisms at the population level. It has also shifted the focus of the analysis of neural activity from quantifying single-neuron correlates with different movement parameters to probing the structure of multi-neuron activity patterns to identify the emergent computational properties of cortical neural circuits. In particular, recent advances in “dimension reduction” algorithms have attempted to identify specific covariance patterns in multi-neuron activity which are presumed to reflect the underlying computational processes by which neural circuits convert the intention to perform a particular movement into the required causal descending motor commands. These analyses have led to many new perspectives and insights on how cortical motor circuits covertly plan and prepare to initiate a movement without causing muscle contractions, transition from preparation to overt execution of the desired movement, generate muscle-centered motor output commands, and learn new motor skills. Progress is also being made to import optical-imaging and optogenetic toolboxes from rodents to non-human primates to overcome some technical limitations of multi-electrode recording technology.
Highlights
For many years, neural recording studies of the cerebral cortical control of voluntary movements in awake, behaving animals were dominated by attempts to correlate the task-related activity of single neurons to the externally measurable properties of the executed movements
The development of simultaneous multi-neuron recording technologies and much more powerful computers over the past two decades has dramatically enhanced our ability to study cortical motor-control mechanisms. This has led to translational applications such as brain–machine interfaces (BMIs) that allow non-human primates (NHPs)[1,2,3,4,5,6] and paralyzed patients[7,8,9,10,11] to impose real-time volitional control over computer cursors, robotic neuroprosthetic devices and even their own limb muscles[12] to perform various tasks
Representational models of voluntary motor control When single-electrode neurophysiological studies of cortical motor control began in the 1960s13,14, the field was dominated by “representational” models of brain function, which assumed that the activity of single neurons explicitly expressed specific kinds of information, such as particular properties of a sensory input or motor output
Summary
Neural recording studies of the cerebral cortical control of voluntary movements in awake, behaving animals were dominated by attempts to correlate the task-related activity of single neurons to the externally measurable properties of the executed movements. The level of neural modulation in latent variables associated with object location versus identity shifted progressively in time, so that object location correlates were strongest near the onset of reach and object identity modulations were progressively stronger later in the trial as the hand approached the objects and adjusted its configuration to grasp them These various findings indicate that it should be very informative to extend DR from separate analyses of activity in each cortical motor area to the pooled activity patterns recorded simultaneously in multiple areas of the same monkeys in the same task and using the same DR methods. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
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