Several neural structures are involved in the production and control of volun-tary movements: the premotor and primary motor cortex, the brain stem, the spinal cord, the basal ganglia and the cerebellum. The neural systems that monitor movements of the hand and arm – the limbs which are responsible for piano performance – are of particular interest for the present thesis.
There are three key organizational features of the motor system (Follow-ing Kandelet al., 1992): First, sensory information is very important for the monitoring of movements because it provides a representation of the outside world and our position in it. Sensory inputs from skin, muscles and joints ascend to the thalamus and are relayed to the somatic sensory areas. From there, somatosensory information is transmitted to the motor cortex and is used to modulate motor performance. The second organizational feature is the functioning of the motor system in ahierarchyof control levels. Higher lev-els of processing located in the motor cortex send general motor commands to be executed by the lower levels (brain stem and spinal cord); lower-levels of processing compute the fine details of the generation of movement, such as the force and angle of the joints, and execute them. Each level is provided with sensory information, but the most detailed sensory monitoring goes to the lower levels of the motor hierarchy that monitor the moment-to-moment features of the response. The hierarchical organization makes possible that there is a great flexibility in the movement execution. Finally, there is the parallelfunctioning of the motor system. This feature concerns the different descending pathways from the motor cortex to the spinal cord, direct ones and indirect ones, which largely overlap in their final projection to the mo-toneurons of the spinal cord. The indirect pathways travel from the motor cortex through the brain stem to the spinal cord. The direct ones constitute the corticospinal tract, which consists of monosynaptic connections between the pyramidal cells in the layer V of the pre- and postcentral gyrus in the cortex and the motoneurons on the spinal cord. The motor commands reach the motoneurons in the spinal cord and then go from there to the muscles.
Thecortical regionswhich give origin to the descending motor pathways correspond to the agranular cortex of Brodmann’s regions 4 and the caudal area 6 (Following Nieuwenhuys et al., 2008). Region 4 is located in the precentral gyrus and corresponds to the primary motor cortex (M1), where the big pyramidal cells of Betz are present. Caudal area 6 corresponds to the premotor cortex and consists of multiple premotor areas, as recent studies have revealed (Matelliet al., 1985, 1991). However the number of premotor areas might increase with future studies. The current parcelation of premotor areas delineates six regions in monkeys (F2–F7), although homologue regions have been proposed for the human brain (Nieuwenhuyset al., 2008): F2–F5 are found in the caudal BA6 and are the origins of the corticospinal tract together with M1 and F6–F7, these latter located in the rostral BA6 (Fig. 1.1).
F2 is the caudal part of the dorsal premotor cortex (PMDc), located ante-rior to M1. F3 in the medial hemisphere of area 6 is the supplementary motor cortex (SMA). F4 and F5 are located in ventral area 6 and are the caudal and dorsal parts of the ventral premotor area, respectively (PMVc and PMVd).
Areas F2–F5 are bidirectionally connected with M1 and with some parietal regions, and are therefore also known as theparietal-dependent premotor areas.
They also receive projections from cingulate areas.
In the rostral BA6 are located areas F6 and F7. F6 is anterior to SMA and is termed pre-SMA. F7 corresponds to the rostral part of the dorsal premotor area (PMDr). Both F6 and F7 are connected with M1 indirectly through more caudal premotor areas and receive corticocortical connections from prefrontal regions. Consequently, they are known asprefrontal-dependent premotor areas.
The large-scale organization of the motor cortex is somatotopic, a prop-erty which is maintained at the different hierarchical levels of the motor system. The existing literature describes a rough body map with some over-lap between the representations of different body parts, some fractures in the representations, and some re-representations (Fulton, 1938; Donoghueet al., 1992; Parket al., 2001). The somatotopic maps can be better understood in a statistical way due to the high variability of the maps across animal species and even across individual animals within a specie (Graziano, 2006).
Any complex, behaviorally relevant movement combines muscles from many parts of the body. To account for such a complexity in the movement repertoire, it seems that the neurons in the motor cortex are tuned to avast set of motor patternsthat may be entrained through experience and that may
Figure 1.1: A. The primary motor and premotor areas of the monkey and their connections with the prefrontal, cingulate, and parietal cortices. B. The macaque primary motor cortex (F1) and the premotor areas F2–F7 as defined by Matelliet al.(1985, 1991). The descriptive nomenclature used in this section is also illustrated. C. Proposed homologies between the monkey and human primary motor and premotor areas. Reproduced with permission from Nieuwenhuyset al.(2008).The human central nervous system.Copyrightc2008 Pergamon Press.
reflect the behavioral needs of the animal (Graziano, 2006).
The direct and indirect descending pathways have a lateral and a me-dial/ventral projection to the motor columns in the enlargements of the spinal cord. These projections can be intercalated by spinal interneurons located in the intermediate zone. The indirect descending pathways also have an aminergic projection. Projections terminate also in a somatotopical pattern.
Lateralbrain stem systemsproject contralaterally directly to motoneurons located in the dorsolateral part of the lateral motor column or via interneu-rons of the dorsolateral and central intermediate zone that finally project to the motoneurons. These lateral brain stem pathways control movements of the extremities, especially those of their distal parts (Nieuwenhuyset al., 2008). Medial brain systems terminate, often bilaterally, either directly at motoneurons in the medial motor columns or via spinal interneurons lo-cated in the ventromedial part of the intermediate zone. These medial brain stem pathways exert their actions bilaterally on axial and proximal mus-cles, for example, to control postural and orienting movements of the head (Nieuwenhuyset al., 2008).
The corticospinal tract consists of the lateral and ventral pathways. It originates in the primary motor cortex (BA4), in the caudal premotor areas (caudal BA6) and in the somatic sensory cortex (BA1, 2 and 3). From the million of axons in the corticospinal tract, around 80% of them cross over to the contralateral side in the medulla oblongata (pyramidal decussation) and descend along the lateral corticospinal tract to project predominantly (around 80–90% of them) to the interneurons of the dorsolateral intermediate zone or directly to the motoneurons in the dorsal parts of the lateral columns in the spinal cord. Another 10% axons enter the lateral corticospinal tract on the same side. Finally, 10% of the remaining axons that do not cross descend bilaterally to the medial columns in the spinal cord and constitute the ventral corticospinal tract. Of special interest for the present review is the lateral corticospinal tract, which provides fine motor control of limbs and digits (Kolb and Whishaw, 2003; Nieuwenhuyset al., 2008).
The overlapping of the terminations of the descending motor pathways in the motor columns of the spinal cord, which ultimately innervate the skeletal muscles, is responsible for the reorganization and good recovery of motor function when a part of the system is damaged. Moreover, the
Figure 1.2: A. Lateral corticospinal tract. The lateral tract crosses at the pyramidal decussation and terminates contralaterally in the shaded area of spinal gray matter. B.
Ventral corticospinal tract. The uncrossed pathways terminate bilaterally in the shaded area of spinal gray matter. Reproduced with permission from Kandelet al.(1992).Principles of Neural Science. Copyright c1992 Mc-Graw Hill.
corticospinal tract enables agility and speed, as well as fractionation and independence of the movements, which is the key to fine motor control.
In non-human primates and humans the corticospinal tract is much more evolved than the lateral brain stem systems and therefore takes over control of distal movements of the hand and arm (Kandelet al., 1992).
In addition to the descending brain systems, the cerebellum and the basal ganglia also regulate motor control through the cerebello–thalamocortical and basal ganglia–thalamocortical connections. Thecerebellumacts on the motor cortex and the brain stem to monitor their activity and the sensory information they receive from the periphery in order to improve the accuracy of the movements. It has a role both in execution and in sequence control.
For voluntary limb movements, the cerebellum is clearly important for both precision and temporal order in the execution of motor programs (Catalan et al., 1998).
Thebasal gangliareceive inputs from motor and nonmotor areas extending from almost the entire cortex to the striatum. The output of the basal ganglia projects to more than a single cortical area (Akkalet al., 2007). Some models have been proposed for the corticostriatal connectivity and can be character-ized by parallel loops from the cortex to three functional subdivisions of the striatum into associative, motor and limbic loops (Postuma and Dagher, 2006).
As part of the cortico–basal ganglia–thalamocortical loop, the basal ganglia enable the fine tuning of the movement by adjusting the inhibition through the indirect pathway within the basal ganglia, and activation through the direct pathway of the motor commands. This view, however, might be too simplistic because new data have shown thatallstriatal cells project to the external segment of the globus pallidus (GPe, originally considered part of the “indirect pathway”), but that a subpopulation of cellsalsoproject to the internal segment (GPi, as part of the direct pathway, Lévesque and Parent, 2005). Concerning the relevant functions of the basal ganglia within the context of motor control, some existing evidence claims that the basal ganglia can facilitate adaptive motor commands and suppress others, thus having an important role in response selection (Basso and Wurtz, 2002; Frank, 2006).
Moreover, in the cognitive domain the basal ganglia seem to also play a role in decision-making (Middleton and Strick, 2000). These findings are of particular interest because they link the basal ganglia to action-monitoring and conflict-monitoring.
I can now summarize the findings that associate thehigher levelsof motor control in the cortex with the voluntary complex movements of the arm and hand. The exact functions of the premotor and motor areas are still under debate, and a major revision of the classical cortical hierarchical view is required (Nieuwenhuyset al., 2008; Graziano, 2006). According to that view, premotor areas control various high-order aspects of movement; the primary motor cortex decomposes movement into simple components in a body map; and these simple movement components are then communicated to the spinal cord for execution. Recently, however, Graziano (2006) found that complex movements are generated when stimulating with long impulse trains the M1 and caudal sector of premotor cortex. This evidence thus casts some doubts on the previous simplistic view of M1.
The M1 (and the primary sensory cortex S1) is always activated by volun-tary movement, and therefore has long been envisioned as having primarily an executive role (Catalanet al., 1998). However, this traditional view of M1 has been challenged by new data showing that the M1 hand area contains subregions that are related to preparatory activity and subregions that change their activity with the learning of new motor skills (Kawashimaet al., 1994).
The SMA is also frequently activated during the execution of movements, but in addition is activated by movement initiation in humans (Orgogozo and Larsen, 1979; Deiberet al., 1996). SMA might take part in the prepara-tion of internally referenced or remembered motor acts (Catalanet al., 1998;
Shibasakiet al., 1993; Sadatoet al., 1996). Nevertheless, its precise role remains elusive (Nieuwenhuyset al., 2008).
The premotor cortex (PMC) is activated by motor tasks involving the generation of sequences from memory (Halsbandet al., 1993; Shibasakiet al., 1993), motor learning (Jenkinset al., 1994) and selection of movement (Deiber et al., 1991).
Both the SMA and the PMC have been reported to play an important role in the generation of motor sequences from memory that fit into a precise timing plan and which have increased complexity (Orgogozo and Larsen, 1979; Rolandet al., 1980; Graftonet al., 1992; Halsbandet al., 1993; Raoet al., 1993; Shibasakiet al., 1993). In the processing of complex sequential finger movements, both the SMA and the contralateral M1 are involved (Gerloff et al., 1997).
As mentioned earlier, the premotor pre-SMA and PMDr do not project
directly to the primary motor cortex and thus may be less closely related to the motor output (Dum and Strick, 2005; Luet al., 1994; Tachibanaet al., 2004).
PMDr is involved in movement selection and coding object locations for orienting and coordinating arm-body movements (Nieuwenhuyset al., 2008).
Pre-SMA is activated by higher order movements which require learning (Picard and Strick, 1996; Nieuwenhuyset al., 2008), prior to the execution of movement sequences (Nachevet al., 2008). Additionally, the pre-SMA is activated during nonmotor, cognitive tasks such as in conflict-monitoring (Nachevet al., 2008).
In sum, despite the several findings of activations of the motor and pre-motor areas in pre-motor and nonpre-motor tasks, further investigations are required to enable a better understanding of their precise functions.