Cortical basis for skilled vocalization.

Marmosets display remarkable vocal motor abilities. Macaques do not. What is it about the marmoset brain that enables its skill in the vocal domain? We examined the cortical control of a laryngeal muscle that is essential for vocalization in both species. We found that, in both monkeys, multiple premotor areas in the frontal lobe along with the primary motor cortex (M1) are major sources of disynaptic drive to laryngeal motoneurons. Two of the premotor areas, ventral area 6 (area 6V) and the supplementary motor area (SMA), are a substantially larger source of descending output in marmosets. We propose that the enhanced vocal motor skills of marmosets are due, in part, to the expansion of descending output from these premotor areas.

The Cortical Motor Areas and the Emergence of Motor Skills: A Neuroanatomical Perspective.

What changes in neural architecture account for the emergence and expansion of dexterity in primates? Dexterity, or skill in performing motor tasks, depends on the ability to generate highly fractionated patterns of muscle activity. It also involves the spatiotemporal coordination of activity in proximal and distal muscles across multiple joints. Many motor skills require the generation of complex movement sequences that are only acquired and refined through extensive practice. Improvements in dexterity have enabled primates to manufacture and use tools and humans to engage in skilled motor behaviors such as typing, dance, musical performance, and sports. Our analysis leads to the following synthesis: The neural substrate that endows primates with their enhanced motor capabilities is due, in part, to (a) major organizational changes in the primary motor cortex and (b) the proliferation of output pathways from other areas of the cerebral cortex, especially from the motor areas on the medial wall of the hemisphere.

Posterior parietal cortex contains a command apparatus for hand movements.

Mountcastle and colleagues proposed that the posterior parietal cortex contains a "command apparatus" for the operation of the hand in immediate extrapersonal space [Mountcastle et al. (1975) J Neurophysiol 38(4):871-908]. Here we provide three lines of converging evidence that a lateral region within area 5 has corticospinal neurons that are directly linked to the control of hand movements. First, electrical stimulation in a lateral region of area 5 evokes finger and wrist movements. Second, corticospinal neurons in the same region of area 5 terminate at spinal locations that contain last-order interneurons that innervate hand motoneurons. Third, this lateral region of area 5 contains many neurons that make disynaptic connections with hand motoneurons. The disynaptic input to motoneurons from this portion of area 5 is as direct and prominent as that from any of the premotor areas in the frontal lobe. Thus, our results establish that a region within area 5 contains a motor area with corticospinal neurons that could function as a command apparatus for operation of the hand.

Subdivisions of primary motor cortex based on cortico-motoneuronal cells.

We used retrograde transneuronal transport of rabies virus from single muscles of rhesus monkeys to identify cortico-motoneuronal (CM) cells in the primary motor cortex (M1) that make monosynaptic connections with motoneurons innervating shoulder, elbow, and finger muscles. We found that M1 has 2 subdivisions. A rostral region lacks CM cells and represents an "old" M1 that is the standard for many mammals. The descending commands mediated by corticospinal efferents from old M1 must use the integrative mechanisms of the spinal cord to generate motoneuron activity and motor output. In contrast, a caudal region of M1 contains shoulder, elbow, and finger CM cells. This region represents a "new" M1 that is present only in some higher primates and humans. The direct access to motoneurons afforded by CM cells enables the newly recognized M1 to bypass spinal cord mechanisms and sculpt novel patterns of motor output that are essential for highly skilled movements.

Muscle representation in the macaque motor cortex: an anatomical perspective.

How are the neurons that directly influence the motoneurons of a muscle distributed in the primary motor cortex (M1)? To answer this classical question we used retrograde transneuronal transport of rabies virus from single muscles of macaques. This enabled us to define cortico-motoneuronal (CM) cells that make monosynaptic connections with the motoneurons of the injected muscle. We examined the distribution of CM cells that project to motoneurons of three thumb and finger muscles. We found that the CM cells for these digit muscles are restricted to the caudal portion of M1, which is buried in the central sulcus. Within this region of M1, CM cells for one muscle display a remarkably widespread distribution and fill the entire mediolateral extent of the arm area. In fact, CM cells for digit muscles are found in regions of M1 that are known to contain the shoulder representation. The cortical territories occupied by CM cells for different muscles overlap extensively. Thus, we found no evidence for a focal representation of single muscles in M1. Instead, the overlap and intermingling among the different populations of CM cells may be the neural substrate to create a wide variety of muscle synergies. We found two additional surprising results. First, 15-16% of the CM cells originate from area 3a, a region of primary somatosensory cortex. Second, the size range of CM cells includes both "fast" and "slow" pyramidal tract neurons. These observations are likely to lead to dramatic changes in views about the function of the CM system.