General
- Occur after unilateral resection of the SMA.
- Global akinesia with normo- or hyporeflexia and a normal tonus, more profound on the contralesional side, while muscle strength can be preserved
- Sensory functions remain undisturbed.
- Symptoms completely resolve within weeks to months, only leaving a disturbance in alternating bimanual movements as the remaining deficit
Anatomy
- SMA or SMA proper (Brodmann area 6) is localised in the posterior part of the superior frontal gyrus
- Borders
- Inferior border
- Cingulate sulcus and gyrus
- Posterior border
- Precentral sulcus separating it from the leg area of the primary motor cortex.
- The lateral and anterior borders are less clearly demarcated on macro-anatomical criteria
- Histochemical and cytoarchitectonic differences have been well described
- Anterior border
- The SMA can be distinguished from the pre-SMA
- Vertical traversing the anterior commissure as a border
- Lateral border
- Dorsal premotor cortex in each hemisphere
- SMA has a somatotopical organization
- Anterior → Posterior
- Face →Arm → Legs are represented in an anteroposterior direction in the SMA.
- In the dominant hemisphere, language seems to be represented most anteriorly
- Connections
- About ten percent of the input from the corticospinal tracts originates in the SMA
- Connections with motor circuits through its connections with the primary motor cortex, premotor cortex and cingulate cortex
- Connections with the superior parietal lobe, insula, basal ganglia, thalamus, cerebellum and especially with the contralateral SMA
- SMA is also connected with the pars opercularis of the inferior frontal gyrus (Broca’s area) through the frontal aslant tract
- 1 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
- (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.
Symptoms
- Strict lesions of the SMA do not result in a specific class of aphasia.
- Reduced spontaneous speech may occur, predominantly described after resection of the SMA in the dominant hemisphere, though not exclusively
- Reduced spontaneous speech may occur, predominantly described after resection of the SMA in the dominant hemisphere, though not exclusively
Differentiating corticospinal tract injury vs SMA (JSG)
- Corticospinal will loose more of the fine movements of the hand and preserve the gross movement of the shoulder and elbow. SMA preserves the fine movements of the arms and looses gross movements of the shoulder and elbow.
Cause of the SMA syndrome
- Following surgical resection
- Deficits are correlated with
- The extent of resection of functionally active SMA
- The distance from the resected area to the SMA (Nelson et al., 2002), to the precentral sulcus and the cingulate sulcus
- An increased incidence of the SMA syndrome and the severity of symptoms is seen when the anteroposterior extent of resection is larger
- Both a resection larger than 90% and the presence of a low-grade glioma are associated with a higher incidence of the SMA syndrome
- They argued that residual function of the SMA is still present in patients harboring a low-grade glioma, while it is unlikely that the SMA syndrome develops in patients with high-grade gliomas, due to the absence of functional neural tissue inside these tumors
- A very intriguing finding was observed in a patient undergoing awake surgery during which the SMA syndrome occurred with a delay of half an hour after the resection
- The authors suggested that an initial compensation of function is possible due to parallel networks or due to residual activity of an oscillatory loop that supports the execution of function but not its initiation
- They made clear that it is highly unlikely that this syndrome is caused by venous thrombosis or postoperative edema, because symptoms presented too early for that
- A follow-up MRI showed no signs of ischemia or venous thrombosis.
- Oedema is also unlikely because it takes weeks to months for the deficits to restore.
- Infarct
Bimanual movement patterns
- Testing
- Anti-phase bimanual movements
- One hand flexes while the other extends
- In-phase bimanual movements,
- Requiring simultaneous flexion and extension at both wrists, without phase shift.
- Both in-phase and anti-phase movements require synchronisation between the two hands,
- But the anti-phase movements additionally need contralateral movement suppression (of a mirrored movement) and the independence of the two movements.
- Difficulties in alternating bimanual movements persist after SMA syndrome resolves
- Generally is described in the upper limbs and not the lower limbs
- Intact SMA influenced the motor program for both hands
- The bimanual coordination deficit after unilateral lesioning of the SMA (and most likely also including the pre-SMA at that time) was resolved after callosal sectioning,
- Monkeys who had resection of the non-dominant SMA and subsequent callosal section
- Behaved as having two preferred hands
- The hand contralateral to the lesion is the one that seems to be at fault
- Due to alternating bimanual movements are cognitively more demanding than mirror movements.
- There is a preference for simultaneous rather than alternating bimanual movements with increasing frequency of movements
- Such simultaneous movements are more stable and performed more accurately
- The SMA is definitely neither the sole contributor nor specific for bimanual coordination but the SMA syndrome provides evidence that bilateral functioning of the SMA is a requirement for anti-phase movements.
- It has been hypothesized that the opposite SMA rapidly takes over the motor function for both sides of the body
- However, for the execution of bimanual alternating movements function of both SMA’s is necessary.
- 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
- In normal conditions this tonic interhemispheric balance may result in both initiation and inhibition of movements. In:
- SMA syndrome this balance is disturbed, leading to temporary lack of movements (akinesia) of the contralateral limbs and irreversible deficits of bimanual alternating movements.
- 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.
Mechanisms of recovery
- Difficult to understand due to
- Heterogeneity associated with lesion studies
- Cerebral infarcts
- Post tumour resection
- Heterogeneity in clinical symptoms after resections may be caused by variability in preoperative reorganization of function due to brain plasticity.
- Neuroplasticity has been brought up in order to understand the temporary deficits.
- Contralateral SMA region compensation
- A lesion in the SMA leads to more activation of the contralateral SMA
- However, it is uncertain whether this reflects functional compensation or is merely the consequence of decreased transcallosal inhibition from the damaged hemisphere
- In patients with left dominant hemisphere lesions in language areas high-frequency repetitive transcranial magnetic stimulation (rTMS) over the right hemisphere disturbs language function in patients with left dominant hemisphere lesions in language areas, which shows that activation in the contralateral hemisphere truly represents function, rather than mere loss of transcallosal inhibition.
- Others have shown that a preoperative switch in activation to the contralateral healthy SMA is not sufficient to avoid the syndrome, but leads to a faster recovery
- This is supported by the fact that the SMA has strong connections with its contralateral counterpart
- Others have raised that hemispheric dominance of the SMA might be important in predicting postoperative deficits, which could explain why not everyone develops the SMA syndrome after unilateral resection of the SMA.
- However, there is no substantial evidence that provides convincing support for this argument.
- A relation between the side of the resection and incidence of the syndrome has not been described.
- Postoperatively, the functional recruitment of the healthy SMA and premotor cortex seems to compensate for the resection of the SMA
- Preoperative reorganisation of cerebral function
- Does not completely account for the recovery
- Because the reversibility of the SMA syndrome is also seen in patients with acute lesions such as an infarct or patients that undergo surgery for epilepsy.
- It is plausible that the patient population with slow growing lesions and subsequent acute surgical lesion have a tendency to recover faster due to preoperative reorganisation
- Additional functional distortion of the SMA due to the mass effect of tumors.
- A resection alleviates this compression, which uncovers residual function of the affected SMA (if any).
Comparison with impaired/altered SMA function in Parkinson’s disease and tics
PD
- Although PD is a chronic deteriorating disease and the SMA syndrome is acute, some parallels can be seen between these disorders.
- Similarities
- Both treatment with Levodopa (PD) and Apomorphine (SMA) can improve function
- Both have bimanual antiphase alternating movement deficits
- Both preserve inphase movements
- Both disorders can be characterized by akinesia
- Do not seem to have dysfunction of the lateral premotor cortex
- Differences
- PD is caused by a loss of dopaminergic neurons in the pars compacta of the substantia nigra
- At the cortical level, decreased activity of the SMA has been well recognized which can be improved with deep brain stimulation of the subthalamic nucleus or treatment with levodopa
- Thus, the reduced output from the basal ganglia in PD most likely leads to a functionally impaired SMA that can be improved with conventional treatment methods.
Features | PD | SMA syndrome |
Aetiology | Loss of dopaminergic neurons in the pars compacta of the substantia nigra | Damage of the SMA region |
Encouragement | Symptoms improve with encouragement (micrographia, akinetic starting difficulties as the lateral premotor cortex is activated | Deficits cannot be improve with encouragement; the lateral premotor cortex seems to takeover some of the SMA function when the SMA is damaged |
Tics
- Tics, as part of the Tourette syndrome, can be considered as movements that escape voluntary control
- Typically they are preceded by a feeling of urge and can be voluntarily suppressed to some extent
- Patients with Tourette syndrome show an increased resting state activity in the SMA compared to healthy subjects.
- There is a strong correlation in activation between the SMA and primary motor cortex during tics
- Activation of the SMA is positively correlated with tic severity
- The SMA is active before tic onset
- Unclear whether the activity in the SMA is involved in tic generation or that it represents the effort of suppression of a tic.
- Mechanism
- Direct electrical stimulation of the SMA can lead to both
- Inhibition of movement or speech arrest,
- Evoke movements the urge to move or vocalizations
- Similarities
- Both can cause speech arrest and vocalizations
- Echophenomena is present in both Tourette and SMA lesioning with TMS
- Echophenomena: Any of a group of automatic imitative actions performed without explicit awareness of the individual, including echolalia, echopraxia, echographia and so forth
- Eg: if someone hears beeping they may immediately tic 'beep beep beep', or if an alarm goes off a person may start making the same noise as the alarm straight after it has started going off.
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