Indirect, referent control of motor actions underlies directional tuning of neurons

Many neurons of the primary motor cortex (M1) are maximally sensitive to "preferred" hand movement directions and generate progressively less activity with movements away from these directions. M1 activity also correlates with other biomechanical variables. These findings are predominantly interpreted in a framework in which the brain preprograms and directly specifies the desired motor outcome. This approach is inconsistent with the empirically derived equilibrium-point hypothesis, in which the brain can control motor actions only indirectly, by changing neurophysiological parameters that may influence, but remain independent of, biomechanical variables. The controversy is resolved on the basis of experimental findings and theoretical analysis of how sensory and central influences are integrated in the presence of the fundamental nonlinearity of neurons: electrical thresholds. In the presence of sensory inputs, electrical thresholds are converted into spatial thresholds that predetermine the position of the body segments at which muscles begin to be activated. Such thresholds may be considered as referent points of respective spatial frames of reference (FRs) in which neurons, including motoneurons, are centrally predetermined to work. By shifting the referent points of respective FRs, the brain elicits intentional actions. Pure involuntary reactions to perturbations are accomplished in motionless FRs. Neurons are primarily sensitive to shifts in referent directions, i.e., shifts in spatial FRs, whereas emergent neural activity may or may not correlate with different biomechanical variables depending on the motor task and external conditions. Indirect, referent control of posture and movement symbolizes a departure from conventional views based on direct preprogramming of the motor outcome.