Comparison of the Neuronal Activity in the SMA and the Ventral Cingulate Cortex During Prehension in the Monkey

Abstract

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.

Neuronal Activity in the Supplementary Motor Area of Monkeys Adapting to a New Dynamic Environment

“…They found substantially similar percentages in SMA and in the (combined) PMd and PMv. Cadoret and Smith (1997) found similar activation in SMA and in the ventral cingulate motor area in a prehension task.…”

Linear correlation between fractal dimension of EEG signal and handgrip force

“…During the movement period, the execution of the motor task activates a greater number of motor neurons. Especially, the dynamic feature of the task during this period requires additional motor neurons as well as higher discharge rate of the neurons to overcome the inertia of the movement (Buys et al 1986;Cadoret and Smith 1997;Thickbroom et al 1999), adding complexity to the signal, and correspondingly, increasing the FD (Lutzenberger et al 1995). During the holding period, motor neurons are continuously recruited to maintain the task at a certain level of force.…”

Responses of Cerebellar Interpositus Neurons to Predictable Perturbations Applied to an Object Held in a Precision Grip

“…This expectation was surprisingly not confirmed. Using a similar paradigm of predictable perturbations, we explored the supplementary and cingulate motor areas (Cadoret and Smith 1997), the dorsal and ventral premotor areas (Boudreau et al 2001), and the motor cortex itself (Picard and Smith 1992). Although all of these areas yielded modulated activity patterns related to grasping and lifting as well as reflex-like responses to the perturbation, none of these same areas had any significant amount of anticipatory activity resembling neurons in the cerebellar nuclei and the cerebellar cortex.…”

“…During the past several years, we demonstrated that monkeys also show similar adaptive behaviors when confronted with predictable perturbations. However, single-cell recordings of the neuronal discharge in the primary motor cortex (M1), the supplementary motor cortex (SMA), the dorsal and ventral premotor cortex (PMd and PMv), and the cingulate motor area (CMA) related to anticipation of a predictable perturbation has so far failed to find any strong evidence of activity related to these preparatory behaviors (Boudreau et al 2001;Cadoret and Smith 1997;Picard and Smith 1992). To date, the only region where we have found specific anticipatory activity is in cells of the paravermal and hemispheric cerebellar cortex (Dugas and Smith 1992).…”