Cortical networks subserving upper limb movements in primates

Abstract

In all primates, the cortical control of hand and arm movements is initiated and controlled by a network of cortical regions including primary motor cortex (M1), premotor cortex (PMC), and posterior parietal cortex (PPC). These interconnected regions are influenced by inputs from especially visual and somatosensory cortical areas, and prefrontal cortex. Here we discuss recent evidence showing M1, PMC, and PPC can be subdivided into a number of functional zones or domains, including several that participate in guiding and controlling hand and arm movements. Functional zones can be defined by the movement sequences evoked by microstimulation within them, and functional zones related to the same type of movement in all three cortical regions are interconnected. The inactivation of a functional zone in each of the regions has a different impact on motor behavior. Finally, there is considerable plasticity within the networks so that behavioral recoveries can occur after damage to functional zones within a network.

Figure 1

Motor areas of cortex on a dorsolateral view of a Squirrel monkey brain. Primary motor cortex (M1) represents foot and leg, trunk, hand and forelimb, and face movements in a sequence of mediolateral segments. Other motor representations in frontal cortex include the dorsal premotor area, PMD, the ventral premotor area, PMV, the supplementary motor area, SMA, and the frontal eye field, FEF. Within M1, PMV, and PMD, different complex movements can be evoked by electrically stimulating neurons within small “functional zones”. The approximate locations of three such zones, for grasping (G), defensive (D), and reaching (R) movements are shown in M1 and premotor cortex (PMV and PMD). Matching functional zones (G, D, and R) for these and other motor behaviors are found in posterior parietal cortex, with the grasping zone extending into area 2. Somatosensory areas (3a, 3b, 1 and 2, as well as several visual areas, are shown for reference. Based on Gharbawie et al. (2011a).

Figure 2

The proposed functional organization of the hand-forearm segment of M1 in monkeys and other primates. Microstimulation studies have shown that electrical stimulation of a small number of adjacent pyramidal neurons in layer 5 with short bursts of near-threshold pulses evokes simple movements of digits (D), the wrist (W), the elbow (E) or the shoulder (S) from different sites in M1, and that sites for each of these body parts are scattered and repeated within the hand-forelimb segment of M1. Microstimulation with longer bursts of electrical pulses (0.5 sec.) at higher current levels evokes more complex patterns of movements, such as that for reaching (R), grasping (G) or defense of the head and body (D) from larger functional zones (see Figure 1) that would contain a number of motor columns of different types. The complex movement patterns may depend on the short lateral neuronal interconnections within a functional zone that are excitatory or inhibitory. Two pyramidal neurons with intrinsic connections are illustrated for example. Longer lateral connections between functional zones may excite mainly inhibitory neurons, suppressing a tendency for a different complex movement sequence.