Dorsolateral Premotor Cortex

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Premotor cortex is the cortex just anterior to Ml where electrical stimulation evokes movements, but at higher levels of current than in Ml. Premotor cortex also projects much less densely to the spinal cord than Ml. Premotor cortex is generally thinner than Ml, but like Ml it has an indistinct or poorly developed layer 4 and thus is agranular or dysgranular in appearance. Unlike Ml (area 4), premotor cortex lacks a dense population of large pyramidal cells (Betz cells). Brodmann characterized most of this region as area 6. The frontal association cortex just rostral to area 6, generally termed prefrontal cortex, is recognized by the appearance of a distinct layer 4.

Premotor cortex is uniform in neither structure nor function, and it clearly contains several cortical fields. Most investigations distinguish at least two nonprim-ary motor fields: a dorsal premotor area (PMD) and a ventral premotor area (PMV) (Figs. l-3). PMD is agranular in histological appearance, whereas PMV is dysgranular, having a thin granular layer 4. Both PMD and PMV lack a significant number of giant pyramidal cells, which are numerous in Ml. The density of myelinated fibers, the density of reactivity of some metabolic enzymes, and the intensity of some types of immunoreactivity are distributed differently in PMD and PMV. Descending projections from both areas are also differently organized. These areas require different levels of electrical stimulation to evoke movements and have different patterns of movement representation.

PMD is located just anterior to Ml and lateral to the SMA. PMD extends laterally to the level of the frontal eye field. PMD is significantly less responsive to intracortical microstimualtion and has markedly higher thresholds for eliciting muscle contractions than Ml. Electrical stimulation evokes hindlimb movements in medial PMD and forelimb movements in lateral PMD. Although movements of both the proximal and the distal limbs can be evoked from

PMD, proximal limb movements (involving shoulder or shoulder and elbow) are most common. Neurons subserving face and eye movements may be located most laterally, just posterior to the frontal eye field.

PMD may be engaged in movements that require orienting the eyes, head, and trunk toward the target when limb movements are directed toward nearby objects and when posture is adjusted. Neurons in PMD project in such a way that those projecting to spinal cord motor pools for the leg are medial to neurons projecting to spinal cord motor pools for the arm. Anteriorly, PMD borders on prefrontal cortex, where neurons do not project to the spinal cord.

Neurons in PMD typically respond to cues that indicate that a motor response will soon be necessary. The neurons also fire during the waiting period and during the movement. As in Ml, many neurons in PMD are activated during particular movements and during limb movements in a particular direction. Thus, PMD appears to have roles in the preparation and guidance of movements. Important sensory inputs to PMD originate in somatosensory and visuomotor

Figure 3 Proposed locations of primary motor cortex (Ml) and premotor fields in the frontal lobe of humans. Rostral (r) and caudal (c) subdivisions of dorsal premotor cortex (PMD) are indicated, as are the ventral premotor area (PMV), the frontal eye field (FEF), and the dorsal division of supplementary motor area (SMAd). In PMV, the upper limb is represented medial to the face and mouth (UL and OF). Most of Ml is buried in the rostral bank of the central fissure (CS). Previous interpretations have extended Ml further onto the surface of the precentral gyrus to cortex we consider to be PMD.

Figure 3 Proposed locations of primary motor cortex (Ml) and premotor fields in the frontal lobe of humans. Rostral (r) and caudal (c) subdivisions of dorsal premotor cortex (PMD) are indicated, as are the ventral premotor area (PMV), the frontal eye field (FEF), and the dorsal division of supplementary motor area (SMAd). In PMV, the upper limb is represented medial to the face and mouth (UL and OF). Most of Ml is buried in the rostral bank of the central fissure (CS). Previous interpretations have extended Ml further onto the surface of the precentral gyrus to cortex we consider to be PMD.

areas of posterior parietal cortex. PMD is reciprocally connected with PMV, M1, the SMA, and cingulate cortex.

The rostral half of PMD is sometimes distinguished as a separate rostral field, PMDr, because current levels for evoked movements are higher and eye and face movements are sometimes evoked. Moreover, a scattering of Betz cells can be found in caudal PMD, whereas in the rostral PMD such large cells are essentially absent. Both caudal and rostral PMD regions are interconnected and the two areas may function in concert.

The PMV is located immediately anterior to the representation of face and tongue movements in M1. PMV can be distinguished from M1 and PMD by the presence of a thin but distinct internal granular layer 4. A layer 5 containing medium-sized pyramidal cells is prominent. Electrical stimulation of PMV results in forelimb, face, tongue, and eye movements. Hand movements are generally produced from cortex just dorsal to cortex subserving face movements. There is no clear evidence for a region devoted to hindlimb movements. Since the currents needed to evoke the movements can be as low as those for M1, PMV has been included within M1 by some authors.

PMV has been divided into separate rostral and caudal areas based on histological differences and different response properties of neurons or into medial and ventral parts based on differences in cytoarchi-tecture and connectivity. In humans, part of PMV of the left cerebral hemisphere (Fig. 3) may be specialized and is known as Broca's area, which is involved in the motor control of speech.

PMV appears to have a major role in visually guiding arm movements. Neurons in caudal PMV tend to respond to touch on the hand, arm, face, and mouth and to visual objects close to or approaching the hands, arm, face, and mouth. Neurons that respond to touch on the hand or arm have visual receptive fields that move with the hand or arm. Neurons in caudal PMV respond to appropriate sensory stimuli and during reaching and grasping movements. The more rostral part of PMV may be more involved in initiating grasping movements of objects such as bits of food and in bringing them to the mouth. Neurons in rostral PMV tend to respond while an object that is to be grasped, such as a desired food object, is observed and during reaching and grasping. Other neurons in rostral PMV, termed mirror neurons, respond during an action such as grasping a bit of food but also when another individual is observed performing the same action. These mirror neurons may have a role in learning from others by imitation or in mental rehearsal. Some investigators propose that learning by imitation plays an important role in language acquisition in humans. Thus, mirror neurons in ventral motor cortex, especially in the left hemisphere, may have language functions in humans. In monkeys, lesions of PMV disturb visually guided reaching movements. PMV's role in guiding reaching movements may depend on its inputs from visuomotor areas in posterior parietal cortex and somatosensory parts of the lateral sulcus. PMV also has connections with M1, PMD, SMA, and cingulate cortex as well as direct projections to the cervical spinal cord, in which motor neurons subserve arm and hand movements.

The dorsolateral premotor region also contains an area with visuomotor functions, the frontal eye field (FEF), which is located just rostral to the junction of PMD and PMV (Figs. 1 and 3). Electrical stimulation within the FEF evokes either saccadic or smooth-pursuit eye movements. The subregion for smooth-pursuit movements is caudal to the subregion for saccadic movements. The FEF receives inputs from a number of visuomotor areas in the temporal and parietal lobes, from adjoining regions of prefrontal cortex, and from frontal visuomotor regions such as the supplementary eye field. Important outputs are to the superior colliculus and to brain stem visuomotor nuclei.

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