New concepts of the supplementary motor area

The supplementary motor area, although traditionally defined as a single motor area, is not viewed as including at least three different areas that can be distinguished anatomically and physiologically. The differential use of these three areas for various motor behaviors has been the subject of recent studies that are beginning to provide novel concepts of the functional differentiation of each area.     

Motor control: exploring the neurochemistry of subliminal inhibition

A new study links individual differences in unconsciously triggered motor control to variability in GABA neurotransmitter concentration in the supplementary motor area of the human brain.     

Implicit Target Substitution and Sequencing for Lexical Tone Production in Chinese: An fMRI Study

In this study, we examine the neural substrates underlying Tone 3 sandhi and tone sequencing in Mandarin Chinese using fMRI. Tone 3 sandhi is traditionally described as the substitution of Tone 3 with Tone 2 when followed by another Tone 3 (i.e., 33→23). According to current speech production models, target substitution is expected to engage the posterior inferior frontal gyrus. Since Tone 3 sandhi is, to some extent, independent of segments, which makes it more similar to singing, right-lateralized activation in this region was predicted. As for tone sequencing, based on studies in sequencing, we expected the involvement of the supplementary motor area. In the experiments, participants were asked to produce twelve four-syllable sequences with the same tone assignment (the repeated sequences) or a different tone assignment (the mixed sequences). We found right-lateralized posterior inferior frontal gyrus activation for the sequence 3333 (Tone 3 sandhi) and left-lateralized activation in the supplementary motor area for the mixed sequences (tone sequencing). We proposed that tones and segments could be processed in parallel in the left and right hemispheres, but their integration, or the product of their integration, is hosted in the left hemisphere.     

Does the supplementary motor area play a part in modifying motor cortex reflexes?

Neuronal activity in the supplementary motor area was recorded from a monkey performing a trained motor task that required readiness for proper usage of sensory inputs. Thirty-two neurons exhibited activity changes, which supports the hypothesis that the SMA is part of the system involved in modulating responsiveness of the motor cortex to sensory inputs in association with learned movements.     

Cerebral haemodynamics during motor imagery of self-feeding with chopsticks: differences between dominant and non-dominant hand

Abstract

Purpose: Motor imagery is defined as a dynamic state during which a subject mentally simulates a given action without overt movements. Our aim was to use near-infrared spectroscopy to investigate differences in cerebral haemodynamics during motor imagery of self-feeding with chopsticks using the dominant or non-dominant hand.

Materials and methods: Twenty healthy right-handed people participated in this study. The motor imagery task involved eating sliced cucumber pickles using chopsticks with the dominant (right) or non-dominant (left) hand. Activation of regions of interest (pre-supplementary motor area, supplementary motor area, pre-motor area, pre-frontal cortex, and sensorimotor cortex was assessed.

Results: Motor imagery vividness of the dominant hand tended to be significantly higher than that of the non-dominant hand. The time of peak oxygenated haemoglobin was significantly earlier in the right pre-frontal cortex than in the supplementary motor area and left pre-motor area. Haemodynamic correlations were detected in more regions of interest during dominant-hand motor imagery than during non-dominant-hand motor imagery.

Conclusions: Haemodynamics might be affected by differences in motor imagery vividness caused by variations in motor manipulation.     

Chronotype predicts activity patterns in the neural underpinnings of the motor system during the day

Neuroimaging is increasingly used to study the motor system in vivo. Despite many reports of time-of-day influences on motor function at the behavioral level, little is known about these influences on neural motor networks and their activations recorded in neuroimaging. Using functional magnetic resonance imaging (fMRI), the authors studied 15 healthy subjects (9 females; mean ± SD age: 23 ± 3 yrs) performing a self-paced finger-tapping task at different times of day (morning, midday, afternoon, and evening). Blood-oxygenation-level-dependent signal showed systematic differences across the day in task-related motor areas of the brain, specifically in the supplementary motor area, parietal cortex, and rolandic operculum (p(corr)< .0125). The authors found that these time-of-day-dependent hemodynamic modulations are associated with chronotype and not with homeostatic sleep pressure. These results show that consideration of time-of-day for the analysis of fMRI studies is imperative.     

Functional magnetic resonance imaging of the primary motor cortex in humans: response to increased functional demands

Functional magnetic resonance imaging (fMRI) studies have been performed on 20 right handed volunteers at 1.5 Tesla using echo planar imaging (EPI) protocol. Index finger tapping invoked localized activation in the primary motor area. Consistent and highly reproducible activation in the primary motor area was observed in six different sessions of a volunteer over a period of one month. Increased tapping rate resulted in increase in the blood oxygenation level dependent (BOLD) signal intensity as well as the volume/area of activation (pixels) in the contra-lateral primary motor area up to tapping rate of 120 taps/min (2 Hz), beyond which it saturates. Activation in supplementary motor area was also observed. The obtained results are correlated to increased functional demands.     

Supplementary motor area of the monkey: activity of neurones during performance of a learned motor task.

1. Recordings were made of the natural dischages of neurones in the supplementary motor area (SMA) of conscious monkeys trained to perform a stereotyped motor task with either hand. 2. Eighty % of the total population of cells showed modulation of their activity during particular movements of either limb. Two thirds of this group had a similar pattern of modulation regardless of whether the contralateral or ipsilateral hand was used. 3. The number of cells whose activity was related to movements of distal joints was approximately equal to that whose discharges occurred with proximal movements. 4. Only 5% of cells tested sent their axons into the pyramidal tract, and only 15% of units investigated showed responses to passive manipulation of the limbs. The effective afferent input usually was of a rather complex kind. 5. The findings suggest that the discharges of a large number of neurones in SMA are changing during particular movements of either arm, and that only a small number of cells receive afferent sensory input. These results contrast with those obtained in the primary motor area and suggest a different role for SMA the control of movement.     

Functional inter-cortical connectivity among motor-related cortices during motor imagery: A magnetoencephalographic study

Neural connectivity was measured during motor imagery (MI) and motor execution (ME) using magnetoencephalography in nine healthy subjects, MI, and at rest. Lower coherence values during ME and MI between sensorimotor areas than at rest, and lower values during MI between the left supplementary motor area and inferior frontal gyrus than ME suggested the sensorimotor network of MI functioned with similar connectivity to ME and that the inhibitory activity functioned continuously during MI, respectively.     

Human medial frontal cortex mediates unconscious inhibition of voluntary action

Within the medial frontal cortex, the supplementary eye field (SEF), supplementary motor area (SMA), and pre-SMA have been implicated in the control of voluntary action, especially during motor sequences or tasks involving rapid choices between competing response plans. However, the precise roles of these areas remain controversial. Here, we study two extremely rare patients with microlesions of the SEF and SMA to demonstrate that these areas are critically involved in unconscious and involuntary motor control. We employed masked-prime stimuli that evoked automatic inhibition in healthy people and control patients with lateral premotor or pre-SMA damage. In contrast, our SEF/SMA patients showed a complete reversal of the normal inhibitory effect--ocular or manual--corresponding to the functional subregion lesioned. These findings imply that the SEF and SMA mediate automatic effector-specific suppression of motor plans. This automatic mechanism may contribute to the participation of these areas in the voluntary control of action.     

Does the Supplementary Motor Area Keep Patients with Ondine's Curse Syndrome Breathing While Awake?

Background

Congenital central hypoventilation syndrome (CCHS) is a rare neuro-respiratory disorder associated with mutations of the PHOX2B gene. Patients with this disease experience severe hypoventilation during sleep and are consequently ventilator-dependent. However, they breathe almost normally while awake, indicating the existence of cortical mechanisms compensating for the deficient brainstem generation of automatic breathing. Current evidence indicates that the supplementary motor area plays an important role in modulating ventilation in awake normal humans. We hypothesized that the wake-related maintenance of spontaneous breathing in patients with CCHS could involve supplementary motor area.

Methods

We studied 7 CCHS patients (5 women; age: 20–30; BMI: 22.1±4 kg.m⁻²) during resting breathing and during exposure to carbon dioxide and inspiratory mechanical constraints. They were compared with 8 healthy individuals. Segments of electroencephalographic tracings were selected according to ventilatory flow signal, from 2.5 seconds to 1.5 seconds after the onset of inspiration. After artefact rejection, 80 or more such segments were ensemble averaged. A slow upward shift of the EEG signal starting between 2 and 0.5 s before inspiration (pre-inspiratory potential) was considered suggestive of supplementary motor area activation.

Results

In the control group, pre-inspiratory potentials were generally absent during resting breathing and carbon dioxide stimulation, and consistently identified in the presence of inspiratory constraints (expected). In CCHS patients, pre-inspiratory potentials were systematically identified in all study conditions, including resting breathing. They were therefore significantly more frequent than in controls.

Conclusions

This study provides a neurophysiological substrate to the wakefulness drive to breathe that is characteristic of CCHS and suggests that the supplementary motor area contributes to this phenomenon. Whether or not this “cortical breathing” can be taken advantage of therapeutically, or has clinical consequences (like competition with attentional resources) remains to be determined.     

Motor mechanisms in speech ontogeny: phylogenetic, neurobiological and linguistic implications

The rhythmic mandible-generated close-open alternations of the mouth, responsible for the series of consonant-vowel alternations characteristic of babbling and of languages, is receiving increased attention as a possible manifestation of an ontogenetic and phylogenetic 'frame' underlying the serial organization of speech. The supplementary motor area appears important for production of this consonant-vowel frame in adults.     

Localization of functional regions of human mesial cortex by somatosensory evoked potential recording and by cortical stimulation

We describe methods of localizing functional regions of the mesial wall, based on 47 patients studied intraoperatively or following chronic implantation of subdural electrodes. Somatosensory evoked potentials were recorded to stimulation of posterior tibial, dorsal pudendal, median, and trigeminal nerves. Bipolar cortical stimulation was performed, and in 4 cases movement-related potentials were recorded.The cingulate and marginal sulci formed the inferior and posterior borders of the sensorimotor areas and the supplementary motor area (SMA). The foot sensory area occupied the posterior paracentral lobule, while the genitalia were represented anterior to the foot sensory area, near the cingulate sulcus. The foot motor area was anterior and superior to the sensory areas, but there was overlap in these representations. There was a rough somatotopic organization within the SMA, with the face represented anterior to the hand. However, there was little evidence of the “pre-SMA” region described in monkeys. Complex movements involving more than one extremity were elicited by stimulation of much of the SMA. The region comprising the supplementary sensory area was not clearly identified, but may involve much of the precuneus. Movement-related potentials did not provide additional localizing information, although in some recordings readiness potentials were recorded from the SMA that appeared to be locally generated.     

Mirroring Pain in the Brain: Emotional Expression versus Motor Imitation

Perception of pain in others via facial expressions has been shown to involve brain areas responsive to self-pain, biological motion, as well as both performed and observed motor actions. Here, we investigated the involvement of these different regions during emotional and motor mirroring of pain expressions using a two-task paradigm, and including both observation and execution of the expressions. BOLD responses were measured as subjects watched video clips showing different intensities of pain expression and, after a variable delay, either expressed the amount of pain they perceived in the clips (pain task), or imitated the facial movements (movement task). In the pain task condition, pain coding involved overlapping activation across observation and execution in the anterior cingulate cortex, supplementary motor area, inferior frontal gyrus/anterior insula, and the inferior parietal lobule, and a pain-related increase (pain vs. neutral) in the anterior cingulate cortex/supplementary motor area, the right inferior frontal gyrus, and the postcentral gyrus. The ‘mirroring’ response was stronger in the inferior frontal gyrus and middle temporal gyrus/superior temporal sulcus during the pain task, and stronger in the inferior parietal lobule in the movement task. These results strongly suggest that while motor mirroring may contribute to the perception of pain expressions in others, interpreting these expressions in terms of pain content draws more heavily on networks involved in the perception of affective meaning.     

Abnormal Movement Preparation in Task-Specific Focal Hand Dystonia

Electrophysiological and behavioral studies in primary dystonia suggest abnormalities during movement preparation, but this crucial phase preceding movement onset has not yet been studied specifically with functional magnetic resonance imaging (fMRI). To identify abnormalities in brain activation during movement preparation, we used event-related fMRI to analyze behaviorally unimpaired sequential finger movements in 18 patients with task-specific focal hand dystonia (FHD) and 18 healthy subjects. Patients and controls executed self-initiated or externally cued prelearnt four-digit sequential movements using either right or left hands. In FHD patients, motor performance of the sequential finger task was not associated with task-related dystonic posturing and their activation levels during motor execution were highly comparable with controls. On the other hand reduced activation was observed during movement preparation in the FHD patients in left premotor cortex / precentral gyrus for all conditions, and for self-initiation additionally in supplementary motor area, left mid-insula and anterior putamen, independent of effector side. Findings argue for abnormalities of early stages of motor control in FHD, manifesting during movement preparation. Since deficits map to regions involved in the coding of motor programs, we propose that task-specific dystonia is characterized by abnormalities during recruitment of motor programs: these do not manifest at the behavioral level during simple automated movements, however, errors in motor programs of complex movements established by extensive practice (a core feature of FHD), trigger the inappropriate movement patterns observed in task-specific dystonia.     

Functional Magnetic Resonance Imaging Connectivity Analyses Reveal Efference-Copy to Primary Somatosensory Area,BA2

Some theories of motor control suggest efference-copies of motor commands reach somatosensory cortices. Here we used functional magnetic resonance imaging to test these models. We varied the amount of efference-copy signal by making participants squeeze a soft material either actively or passively. We found electromyographical recordings, an efference-copy proxy, to predict activity in primary somatosensory regions, in particular Brodmann Area (BA) 2. Partial correlation analyses confirmed that brain activity in cortical structures associated with motor control (premotor and supplementary motor cortices, the parietal area PF and the cerebellum) predicts brain activity in BA2 without being entirely mediated by activity in early somatosensory (BA3b) cortex. Our study therefore provides valuable empirical evidence for efference-copy models of motor control, and shows that signals in BA2 can indeed reflect an input from motor cortices and suggests that we should interpret activations in BA2 as evidence for somatosensory-motor rather than somatosensory coding alone.     

Processing of visually presented sentences in Mandarin and English studied with fMRI.

Comprehension of visually presented sentences in fluent bilinguals was studied with functional magnetic resonance imaging (fMRI) using a set of conceptually similar sentences in two orthographically and phonologically distinct languages, Mandarin and English. Responses were monitored during scanning. Sentence comprehension in each language was compared to fixation in nine subjects and Tamil-like pseudo-word strings in five subjects. Spatially congruent activations in the prefrontal, temporal, and superior parietal regions and in the anterior supplementary motor area were observed for both languages and in both experiments at the individual and group levels of analysis. Proficient bilinguals exposed to both languages early in life utilize common neuroanatomical regions during the conceptual and syntactic processing of written language irrespective of their differences in surface features.     

A Comparison of the Ipsilateral Cortical Projections to the Dorsal and Ventral Subdivisions of the Macaque Premotor Cortex

The cortical connections of the dorsal (PMd) and ventral (PMv) subdivisions of the premotor area (PM, lateral area 6) were studied in four monkeys (Macaca fascicularis) through the use of retrograde tracers. In two animals, tracer was injected ventral to the arcuate sulcus (PMv), in a region from which forelimb movements could be elicited by intracortical microstimulation (ICMS). Tracer injections dorsal to the arcuate sulcus (PMd) were made in two locations. In one animal, tracer was injected caudal to the genu of the arcuate sulcus (in caudal PMd [cPMd], where ICMS was effective in eliciting forelimb movements); in another animal, it was injected rostral to the genu of the arcuate sulcus (in rostral PMd [rPMd], where ICMS was ineffective in eliciting movements). Retrogradely labeled neurons were counted in the ipsilateral hemisphere and located in cytoarchitectonically identified areas of the frontal and parietal lobes. Although both PMv and PMd were found to receive inputs from other motor areas, the prefrontal cortex, and the parietal cortex, there were differences in the topography and the relative strength of projections from these areas.

There were few common inputs to PMv and PMd; only the supplementary eye fields projected to all three areas studied. Interconnections within PMd or PMv appeared to link hindlimb and forelimb representations, and forelimb and face representations; however, connections between PMd and PMv were sparse. Areas cPMd and PMv were found to receive inputs from other motor areas—the primary motor area, the supplementary motor area, and the cingulate motor area—but the topography and strength of projections from these areas varied. Area rPMd was found to receive sparse inputs, if any, from these motor areas. The frontal eye field (area 8a) was found to project to PMv and rPMd, and area 46 was labeled substantially only from rPMd. Parietal projections to PMv were found to originate from a variety of somatosensory and visual areas, including the second somatosensory cortex and related areas in the parietal operculum of the lateral sulcus, as well as areas 5, 7a, and 7b, and the anterior intraparietal area. By contrast, projections to cPMd arose only from area 5. Visual areas 7m and the medial intraparietal area were labeled from rPMd. Relatively more parietal neurons were labeled after tracer injections in PMv than in PMd. Thus, PMv and PMd appear to be parts of separate, parallel networks for movement control.     

Optimal Representation of Supplementary Variables in Biplots from Principal Component Analysis and Correspondence Analysis

This paper treats the topic of representing supplementary variables in biplots obtained by principal component analysis (PCA) and correspondence analysis (CA). We follow a geometrical approach where we minimize errors that are obtained when the scores of the PCA or CA solution are projected onto a vector that represents a supplementary variable. This paper shows that optimal directions for supplementary variables can be found by solving a regression problem, and justifies that earlier formulae from Gabriel are optimal in the least squares sense. We derive new results regarding the geometrical properties, goodness of fit statistics and the interpretation of supplementary variables. It is shown that supplementary variables can be represented by plotting their correlation coefficients with the axes of the biplot only when the proper type of scaling is used. We discuss supplementary variables in an ecological context and give illustrations with data from an environmental monitoring survey.     

Regional Brain Atrophy and Functional Connectivity Changes Related to Fatigue in Multiple Sclerosis

Fatigue is one of the most frequent symptoms in multiple sclerosis (MS), and recent studies have described a relationship between the sensorimotor cortex and its afferent and efferent pathways as a substrate of fatigue. The objectives of this study were to assess the neural correlates of fatigue in MS through gray matter (GM) and white matter (WM) atrophy, and resting state functional connectivity (rs-FC) of the sensorimotor network (SMN). Eighteen healthy controls (HCs) and 60 relapsing-remitting patients were assessed with the Fatigue Severity Scale (FSS). Patients were classified as fatigued (F) or nonfatigued (NF). We investigated GM and WM atrophy using voxel-based morphometry, and rs-FC changes with a seed-based method and independent component analysis (ICA). F patients showed extended GM and WM atrophy focused on areas related to the SMN. High FSS scores were associated with reductions of WM in the supplementary motor area. Seed analysis of GM atrophy in the SMN showed that HCs presented increased rs-FC between the primary motor and somatosensory cortices while patients with high FSS scores were associated with decreased rs-FC between the supplementary motor area and associative somatosensory cortex. ICA results showed that NF patients presented higher rs-FC in the primary motor cortex compared to HCs and in the premotor cortex compared to F patients. Atrophy reduced functional connectivity in SMN pathways and MS patients consequently experienced high levels of fatigue. On the contrary, NF patients experienced high synchronization in this network that could be interpreted as a compensatory mechanism to reduce fatigue sensation.