Which lobe of the cerebrum is responsible for planning and initiating voluntary motor movement?

Supplementary Motor Area

The supplementary motor area (SMA) occupies the posterior one third of the superior frontal gyrus and is responsible for planning of complex movements of contralateral extremities but ipsilateral planning to a small effect.23 The full “SMA syndrome” involves speech arrest, contralateral weakness, and near-total recovery in weeks to months. For tumors involving the SMA, functional MRI shows ipsilateral decreased SMA activity compensated by increased contralateral activity.24 After resection in the SMA, the motor deficit is further compensated by recruitment of activity in the contralateral SMA and premotor cortex. Typically, leg weakness improves followed by the arm and then speech. There are patients who have reported even 6 months of significant speech trouble before returning to almost normal speech.

IV. Supplementary Motor Cortex

The SMA was first described in the cortex of the medial wall of the frontal lobe of humans more than 50 years ago. In monkeys, SMA extends onto the dorsal surface of the medial frontal lobe just rostral to M1 and medial to PMD (Fig. 1). The area is also known as the medial premotor cortex (MPC). Although SMA is usually considered to be a single area, it has been divided into medial (SMAm) and dorsal (SMAd) subdivisions in monkeys (Fig. 2). SMAm appears to be more densely connected to M1, whereas SMAd is somewhat more myelinated. More consistently, the SMA region has been divided into a SMA-proper (SMAd plus SMAm), located immediately rostral to the mesial sector of M1 representing foot, and a pre-SMA, extending toward prefrontal cortex just anterior to a SMA-proper. Both regions border the agranular cingulate cortex in the cingulate sulcus.

SMA was initially recognized when electrical stimulation of the region evoked movements in humans. SMA has subsequently been described in monkeys and carnivores. The region known as M2 in rats is likely to be SMA. Thus, SMA may be an area that exists in many mammals. Stimulation of posterior SMA evokes movements of the contralateral leg, the middle portion is related to movements of the arm and hand, and the most anterior portion is devoted to the face. Current thresholds for evoking movements are generally higher in SMA than in M1. The internal organization of SMA is like a smaller version of M1. Like M1, similar movements may be elicited from more than one site in SMA. Matching bilateral movements are occasionally evoked from sites in SMA.

SMA is within the medial part of Brodmann's area 6. The cortex is agranular, without an obvious layer 4 of granule cells. The layer 5 pyramidal neurons are generally smaller than in adjoining M1. SMA has dense interconnections with M1 and dense projections to the motor neuron pools in the spinal cord. Inputs include those from visual, somatosensory, and auditory association and multimodal areas of the temporal and parietal lobes. SMA receives major inputs from regions of the thalamus with inputs from the internal segment of the globus pallidus, and a minor input from that part of the thalamus receiving inputs from the cerebellum.

Neurons in SMA respond to visual, auditory, and tactile stimuli when these stimuli are used as signals to start a movement or series of movements. When the signal indicates that a movement must be delayed for a short period of time, SMA neurons respond strongly during the delay period. This is partial evidence that SMA has a role in initiating and planning movements.

SMA was originally thought to have a significant role in coordinating movements of the two hands, partly because electrical stimulation of SMA neurons was once thought to commonly evoke ipsilateral movements. This has proven to be rare, however. During movements of one side of the body, only contralateral SMA shows significant activity. Although connections are strong between the SMA of each cerebral hemisphere, lesions of SMA do not produce deficits that suggest a major role in bimanual coordination. Instead, SMA appears to be important in the initiation of contralateral movements, motor programming, motor planning, and motor learning. After lesions, voluntary movements can be elicited by sensory cues and skilled movements can be executed. However, lesions impair the ability to self-initiate learned movements and sequences of movements when no sensory cue indicates the time for movement onset.

Pre-SMA is a small region of cortex just rostral to SMA. Movements are usually not evoked by electrical stimulation of pre-SMA unless much higher current levels are used and a series of current pulses of longer duration are employed. Pre-SMA lacks direct connections with M1, and it does not project or projects very weakly to motor neurons in the spinal cord. Pre-SMA has strong connections with prefrontal cortex, SMA, and cingulate motor areas. Neurons in pre-SMA are preferentially active prior to movement, and they respond less frequently to somatosensory stimuli but more frequently to visual stimuli. Pre-SMA is thought to be involved in the more cognitive aspects of motor behavior, possibly in updating motor plans and in the learning of new motor sequences.

In addition to somatomotor areas, a separate oculomotor area, the supplementary eye field (SEF), is found in the dorsomedial frontal cortex. SEF lies rostrolateral to the SMA and pre-SMA, and it is distinguishable from these two areas by its close relation to eye movements and its anatomical connections with cortical and subcortical oculomotor centers.

Supplementary and preSMAs

The SMA is a portion of the premotor cortex located on the medial surface of the cortex anterior to the precentral sulcus. It is composed of at least two subregions that can be distinguished on the basis of cytoarchitecture, connectivity, and function: the preSMA, which lies anterior to the vertical line passing through the anterior commissure and the SMA proper (or simply SMA) located posterior to this line (Picard & Strick, 1996). Primate neurophysiological studies have suggested that the preSMA and SMA are differentially involved in the sequencing and initiation of movements, with the preSMA acting at a more abstract level than the more motoric SMA (Matsuzaka, Aizawa, & Tanji, 1992; Shima, Mushiake, Saito, & Tanji, 1996; Shima & Tanji, 1998, 2000; Tanji, 2001; Tanji & Shima, 1994). These areas also have distinct patterns of connectivity with cortical and subcortical areas in monkeys (Jürgens, 1984; Luppino, Matelli, Camarda, & Rizzolatti, 1993), a finding supported in humans using diffusion tensor imaging (Johansen-Berg et al., 2004; Lehéricy et al., 2004). The preSMA is heavily connected with the prefrontal cortex and the caudate nucleus, whereas the SMA is more heavily connected with the motor cortex and the putamen, again suggesting a functional breakdown with preSMA involved in higher-level motor planning and SMA with motor execution.

Speech-related symptoms from patients with lesions to the SMA have been described in the literature (e.g., Jonas, 1981, 1987; Pai, 1999; Ziegler, Kilian, & Deger, 1997). These often result in a transient period of total mutism, after which patients may suffer from reduced propositional (self-initiated) speech with nonpropositional speech (automatic speech; e.g., counting and repeating words) nearly intact. Based largely on lesion literature, Jonas (1987) and Ziegler et al. (1997) arrived at similar conclusions regarding the role of the SMA in speech production, suggesting that it aids in sequencing and initiating speech sounds, but likely not in determining their phonemic content.

Recent neuroimaging studies have begun to reveal the distinct contributions made by the SMA and preSMA to speech production. Bohland and Guenther (2006) noted that activity in the preSMA increased for sequences composed of more phonologically complex syllables, whereas activity in the SMA showed no such effect for syllable complexity, but rather, its response was preferentially increased when the sequence was overtly articulated. In a study of word production, Alario, Chainay, Lehericy, and Cohen (2006) provided further evidence for a preferential involvement of the SMA in motor output and suggested a further functional subdivision within the preSMA: The anterior preSMA is more involved with lexical selection and the posterior portion with sequence encoding and execution (see also Tremblay & Gracco, 2006). Collectively, these studies suggest that the SMA is more involved in the initiation and execution of speech output, whereas the preSMA contributes to higher-level processes including lexical selection and sequencing of syllables and phonemes.

Anatomofunctional Organization of Supplementary Motor Area

The supplementary motor area (SMA), namely the frontomesial area located in front of the primary motor area of the inferior limb, is involved in the planning of the movement. Its resection induces the classical “SMA syndrome.” This syndrome is characterized by a complete akinesia and even mutism in cases of lesions of the left dominant SMA, which occurs approximately 30 min following the end of the resection, as observed in awake patients. Then, this syndrome suddenly and spontaneously resolves around the 10th day following surgery, even if some rehabilitation is often needed during 1 to 3 months in order to allow a truly complete functional recovery. Using preoperative fMRI, it has been shown that the occurrence of this syndrome was not related to the volume of the frontal resection, but directly to the removal of a specific structure called the “SMA-proper,” detectable on the preoperative FNI. Thus, on the basis of the presurgical fMRI, it is now possible to predict, before surgery, if an SMA syndrome will occur or not postoperatively, and to inform the patient and his family.17 Moreover, by coupling preoperative fMRI, the pattern of clinical deficit after surgery, and the extent of resection on the postoperative MRI, the existence of a somatotopy within the SMA-proper has been demonstrated—namely, from anterior to posterior: the representation of language (at least in the dominant hemisphere), of the face, then the superior limb, and then the inferior limb (immediately in front of the paracentral lobule). As a consequence, it is also possible to predict before SMA resection the severity and the pattern of the postoperative transient deficit (e.g., only mutism, or mutism and akinesia of the superior limb, or akinesia of the entire hemibody). This has an important impact in planning rehabilitation.

Cortical areas

The SMA and premotor cortex are located in the frontal lobe and implicated in the planning and initiation of voluntary motor movements. In connection with the basal ganglia, the SMA and premotor cortex are activated during beat-based timing, as well as during beat perception (Grahn & Watson, 2013). Furthermore, research indicates that increased coupling between the auditory areas and premotor cortex exist during rhythm processing, particularly of complex rhythmic patterns (Chen et al., 2008; Grahn & Watson, 2013). These findings provide evidence as to the neurologic mechanisms underlying rhythmic entrainment and illustrate how we are able to synchronize our motor movements to a rhythmic pulse.

The voluntary motor loop

Initiation of voluntary actions involves a basal ganglia loop that originates and terminates in the supplementary motor area (SMA) (Fig. 13.13; see also Ch. 3). Activity in the SMA and voluntary motor loop is facilitated by dopamine, which lowers the threshold for movement initiation. This helps to determine whether an intention to act is translated into an actual movement. Reduced activity in the SMA (due to striatal dopamine deficiency) is responsible for the akinesia (poverty of movement) in Parkinson's disease.

The SMA is involved in self-initiated actions (e.g. throwing a ball, rising from a chair) rather than movements that occur in response to an external stimulus or trigger (e.g. catching a ball, stepping over a piece of chalk). This has been exploited with the creation of virtual reality glasses that provide artificial visual cues for parkinsonian patients (projections of horizontal lines to ‘step over’). This leads to improvement in gait initiation, stride length and pace, with fewer falls. In some cases, powerful emotions can overcome akinesia (Clinical Box 13.6).

Key Points

Initiation of voluntary movement is associated with increased activity in the supplementary motor area (SMA) and voluntary motor loop, which is facilitated by dopamine.

The SMA is particularly involved in self-initiated (rather than externally triggered) actions and this type of movement is most affected in Parkinson's disease.

In addition to the well-known (and best-understood) roles in motor control, the basal ganglia also contribute to numerous aspects of cognition, behaviour and mood.

3.28.5.4.3 Differentiation of the supplementary motor area

Studies suggest that a supplementary motor area first appeared with prosimian primates, as evidenced by two distinct SMA motor representations corresponding to distinct cytoarchitecture located on the medial surface of the hemisphere in Galago. These two areas are referred to as SMA-proper and the pre-SMA, situated more rostrally (see figures 4 and 5 in Wu et al., 2000). A supplementary motor area has also been identified in New World monkeys (Gould et al., 1986).

Both SMA and pre-SMA (or areas F3 and F4) have been identified in macaques based on cytoarchitecture, intracortical microstimulation, and connections (Matelli et al., 1991; Matsuzaka et al., 1992; Luppino et al., 1993; Rouiller et al., 1999; Liu et al., 2002; Morel et al., 2005). Compared to SMA, pre-SMA has only sparse spinal projections, and high thresholds for evoking movement, and likely plays less of a direct role in the execution of movement (Luppino et al., 1993; He et al., 1995; Dum and Strick, 1996; Liu et al., 2002). Pre-SMA is thought to have greater involvement in cognitive aspects of motor processing.

55.3.4.1 Comment

The relationship between the SMA and akinesia in parkinsonism has been reviewed by Williams et al. (2002): Activity in the SMA is a major contributor to the Bereitschaftspotential that precedes self‐generated movements and this potential is reduced in PD. Imaging studies confirm impaired activation of SMA during some movements in untreated PD; this is reversible using the dopaminergic agonist apomorphine. It is of interest therefore that our patient showed features similar to the akinesia of parkinsonism following SMA resection, though the more striking abnormality was in loss of bimanual coordination.

Functional Role of the SMA Suggested from the Analysis of Cell Activity

Cells in the SMA are often active when one is initiating or planning to initiate limb movements, regardless of whether the movements are triggered or self-initiated. Activity is observed when an individual is initiating either simple or complex organized movements. These observations led to the view that the SMA is similarly involved in the initiation or preparation of limb movements. However, just because cells in both the SMA and M1 fire on initiation of limb movements, it does not necessarily follow that the functional meaning of the cellular activity is similar. To address this issue, researchers trained monkeys to select three different distal movements: to press a key with the digits of the right or left hand alone or both together. Cells in the M1 are typically active in association with contralateral hand movements. Therefore, the activity accompanying a right-hand key press or bilateral (simultaneous) key press was similar. However, a majority of SMA cells behaved differently. SMA cells were typically active before the initiation of the right-hand key press only (and not before the bilateral key press), or the left-hand key press only, or exclusively when both hands pressed the key together (Figure 2). This implies that the SMA cells are involved in selecting which hand to use rather than selecting muscles in the contralateral limb (as is applicable for M1 cells). It is important to note that an observation of this sort is possible only when experiments are designed rigorously to pursue the aim of the investigation. The proposal that the SMA plays a role in selecting body parts to be used in intended actions was substantiated in a recent report. A separate report proposed a role of the SMA in the temporal organization of multiple movements; SMA cells were found to take part in retrieving the sequences of multiple movements and in temporally connecting one movement to another.

Premotor Area

There is supplementary motor area on and above the superior part of cingulate sulcus on the medial aspect hemisphere that reaches to the premotor cortex (Brodmann areas 6 and 8) on the lateral surface of brain. The cortical area in inferior frontal gyrus corresponds to motor speech area or speech area of Broca (Brodmann areas 44 and 45) and frontal eye area (Fig. 1.8). Lesion into the motor speech area of Broca results in aphasia even the muscles concerned are intact. In 95% of right-handers do have left-hemisphere dominance for language functions, only around 19% of left-handers have right-hemisphere language dominance, with another 20% or so processing language functions in both hemispheres.9