Insights from the supplementary motor area syndrome in balancing movement initiation and inhibition

Abstract

The supplementary motor area (SMA) syndrome is a characteristic neurosurgical syndrome that can occur after unilateral resection of the SMA. Clinical symptoms may vary from none to a global akinesia, predominantly on the contralateral side, with preserved muscle strength and mutism. A remarkable feature is that these symptoms completely resolve within weeks to months, leaving only a disturbance in alternating bimanual movements. In this review we give an overview of the old and new insights from the SMA syndrome and extrapolate these findings to seemingly unrelated diseases and symptoms such as Parkinson's disease (PD) and tics. Furthermore, we integrate findings from lesion, stimulation and functional imaging studies to provide insight in the motor function of the SMA.

Keywords: Parkinson’s disease; akinetic mutism; neurosurgery; supplementary motor area (SMA); supplementary motor area syndrome; tic disorders.

Figure 1

3D view of the probabilistic tractography between both SMA’s from a single healthy subject (made with FSL). The tractography result was transformed to Montreal Neurological Institute (MNI) space. This figure nicely illustrates that the SMA’s are densely interconnected through the corpus callosum.

Figure 2

3D view of the probabilistic tractography between both SMA’s from a single healthy subject (made with FSL). Pre- and postoperative MRI scan of a 64-year-old patient with a diffuse astrocytoma (WHO grade II) in the left SMA. (A) Transversal and coronal T2-weighted FLAIR images, with an SMA template projected on the healthy hemisphere. The latter is freely available and derived from a large meta-analysis describing the location of the sensorimotor areas (Mayka et al., 2006). (B) Transversal images after gadolinium contrast from the same patient before (left lower corner) and three months after the operation (right lower corner). She had a complete motor loss on the right side after the operation, which quickly recovered.

Figure 3

Proposed mechanisms of modulation of the SMA in normal subjects, SMA syndrome, PD and tics. The SMA can both positively and negatively modulate the contralateral SMA (Grefkes et al., 2008). In normal conditions this tonic interhemispheric balance may result in both initiation and inhibition of movements. In the SMA syndrome this balance is disturbed, leading to temporary lack of movements (akinesia) of the contralateral limbs and irreversible deficits of bimanual alternating movements. In PD, activity of both SMA’s is reduced, leading to akinesia and disturbances in bimanual alternating movements. Tics, however, result from bilaterally increased SMA activity. A disturbed interhemispheric balance may either aid in the suppression of tics or mediate the generation of tics. The functional schemes are projected on a coronal MNI brain section. = denotes unchanged modulation, < denotes decreased modulation, > denotes increased modulation.