Comparison of the neuronal activity in the SMA and the ventral cingulate cortex during prehension in the monkey

Two monkeys were trained to use the thumb and forefinger to lift and hold an instrumented apparatus within a narrow position window for 1 s. The device was equipped to measure the position and the grip and lifting forces exerted by the animal. On blocks of trials the weight and surface texture could be varied or a force-pulse perturbation could be systematically delivered 750 ms after the object entered the window. If unopposed, the perturbation would displace the hand from the position window, and in preparation for this perturbation the monkeys either increased their grip force before the perturbation or raised the object higher within the position window. Two clearly separated clusters of cells in the medial wall of the frontal lobe were found to be active in relation to the task. One group of cells (n = 115) was located in the caudal and medial part of area 6, in the supplementary motor area (SMA), and the other (n = 92) was located in the ventral bank of the cingulate sulcus (CMAv), in area 23c. In each area, neurons were characterized by their sensorimotor features clearly related to the hand in addition to their modulated activity in the task. In the SMA, 71% (42 of 59) of the neurons tested for receptive fields responded to peripheral and mainly proprioceptive stimulation, and 71% of them (30 of 42) received inputs from the hand. In the CMAv, 77% (48 of 62) of the neurons responded to peripheral proprioceptive stimulation, and 77% (37 of 48) exhibited receptive fields originating from the hand. Intracortical microstimulation applied to 43 sites in the SMA evoked discrete hand movements at 12 loci, whereas in the CMAv hand movements were observed at 8 of 27 sites tested with an average threshold of > 15 microA. A strong similarity was observed between the SMA and CMAv neurons in their sensorimotor features as well as the modulation of their activity in relation to the prehension task. In both areas the activity was poorly related to grip force and significant correlation with peak grip force was observed for only 9 and 7% of the CMAv and SMA neurons, respectively. In the SMA only five cells exhibited increased activity before the perturbation and in the CMAv no changes in activity were found despite the presence of clear preparatory increases in grip force in anticipation of the perturbation. The perturbation evoked reflexlike excitation of 38% (25 of 65) of the neurons in the CMAv and 28% (20 of 71) of the cells in the SMA; these cells were similar in magnitude and latency (approximately 50 ms) in both areas. In both the SMA and CMAv, most of the neurons increased their firing rate < 200 ms before the grip force onset and the overlap in the distribution of neuronal response times suggests a parallel activation of the SMA and CMAv neurons during the prehension task.