Motor Areas of the Medial Wall: A Review of Their Location and Functional Activation

Our goal in this review is to provide an anatomical frameworkfor the analysis of the motor functions of the medial wall ofthe hemisphere in humans and laboratory primates. Convergingevidence indicates that this region of the frontal lobe containsmultiple areas involved in motor control. In the monkey, themedial wall contains four premotor areas that project directlyto both the primary motor cortex and the spinal cord. Theseare the supplementary motor area (SMA) on the superior frontalgyrus and three motor areas buried within the cingulate sulcus.In addition, there is evidence that a fifth motor field. thepre-SMA. lies rostral to the SMA proper. Recent physiologicalobservations provide evidence for functional differences amongthese motor fields. In the human, no consensus exists on the number of distinctmotor fields on the medial wall. In this review, we summarizethe results of positron emission tomography (PET) studies thatexamined functional activation on the medial wall of humans.Our analysis suggests that it is possible to identify at leastfour separate cortical areas on the medial wall. Each area appearsto be relatively more involved in some aspects of motor behaviorthan others. These cortical areas in the human appear to beanalogous to the pre-SMA, the SMA proper, and two of the cingulatemotor areas of the monkey. We believe that these correspondencesand the anatomical framework we describe will be important forunraveling the motor functions of the medial wall of the hemisphere.     

Interval and ordinal properties of sequences are associated with distinct premotor areas

Lesion and imaging studies have suggested that the premotor cortex (PMC) is a crucial component in the neural network underlying the processing of sequential information. However, whether different aspects of sequential information like interval and ordinal properties are supported by different anatomical regions, and whether the representation of sequential information within the PMC is necessarily related to motor requirements, remain open questions. Brain activations were investigated during a sequence encoding paradigm in 12 healthy subjects using functional magnetic resonance imaging. Subjects had to attend either to the interval or to the ordinal information of a sequence of visually presented stimuli and had to encode the relevant information either before motor reproduction or before perceptual monitoring. Although interval and ordinal information led to activations within the same neural network, direct comparisons revealed significant differences. The pre-supplementary motor area (preSMA), the lateral PMC, the frontal opercular cortex as well as basal ganglia and the left lateral cerebellar cortex (CE) were activated significantly more strongly by interval information, whereas the SMA, the frontal eye field, the primary motor cortex (MI), the primary somatosensory cortex, the cuneus as well as the medial CE and the thalamus were activated more strongly by ordinal information. In addition, serial encoding before reproduction led to higher activations than serial encoding before monitoring in the preSMA, SMA, MI and medial CE. Our findings suggest overlapping but different kinds of sequential representation, depending on both the ordinal and interval aspects as well as motor requirements.     

Somatosensory, motor, and reaching/grasping responses to direct electrical stimulation of the human cingulate motor areas

OBJECT: Surgery for frontal lobe drug-resistant epilepsies is often limited by the apparent widespread distribution of the epileptogenic zone. Recent advances in the parcellation of the medial premotor cortex give the opportunity to reconsider "seizures of the supplementary motor area" (SMA), and to assess the contribution of cingulate motor areas (CMAs), SMA proper (SMAp), and pre-SMA to the symptomatology of premotor seizures. METHODS: The authors reviewed the results of extraoperative electrical stimulation (ES) applied in 52 candidates for epilepsy surgery who underwent stereotactic intracerebral electroencephalographic recordings, focusing on ES of the different medial premotor fields; that is, the anterior and posterior CMA, the SMAp, and the pre-SMA. The ES sites were localized by superposition of the postoperative lateral skull x-ray and the preoperative sagittal MR imaging studies. RESULTS: Among 94 electrodes reaching the medial premotor wall, 57 responses were obtained from the anterior CMA (13 cases), the posterior CMA (11), the pre-SMA (18), and the SMAp (15). The ES of the pre-SMA and SMAp gave rise most often to a combination of motor (31 cases), speech-related (22), or somatosensory (3) elementary symptoms. The ES of the CMA yielded simple (17 of 24) more often than complex responses (7 of 24), among which sensory symptoms (7) were overrepresented. Irrepressible exploratory reaching/grasping movements were elicited at the vicinity of the cingulate sulcus, from the anterior CMA (3 cases) or the pre-SMA (1). Clinical responses to ES were not predictive of the postoperative neurological outcome. CONCLUSIONS: These findings might be helpful in epilepsy surgery candidates, to better target investigation of the CMA, pre-SMA, and SMAp, and therefore to provide a better understanding of premotor seizures.     

Activity in the paracingulate and cingulate sulci during word generation: an fMRI study of functional anatomy.

The supracallosal medial frontal cortex can be divided into three functional domains: a ventral region with connections to the limbic system, an anterior dorsal region with connections to lateral prefrontal systems, and a posterior dorsal region with connections to lateral motor systems. Lesion and functional imaging studies implicate this medial frontal cortex in speech and language generation. The current functional magnetic resonance imaging (fMRI) study of word generation was designed to determine which of these three functional domains was substantially involved by mapping individual subjects' functional activity onto structural images of their left medial frontal cortex. Of 28 neurologically normal right-handed participants, 21 demonstrated a prominent paracingu- late sulcus (PCS), which lies in the anterior dorsal region with connections to lateral prefrontal systems. Activity increases for word generation centered in the PCS in 18 of these 21 cases. The posterior dorsal region also demonstrated significant activity in a majority of participants (16/28 cases). Activity rarely extended into the cingulate sulcus (CS) (3/21 cases) when there was a prominent PCS. If there was no prominent PCS, however, activity did extend into the CS (6/7 cases). In no case was activity present on the crest of the cingulate gyrus, which is heavily connected to the limbic system. Thus, current findings suggest that medial frontal activity during word generation reflects cognitive and motor rather than limbic system participation. The current study demonstrates that suitably designed fMRI studies can be used to determine the functional significance of anatomic variants in human cortex.     

3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum

Studies in non-human primates have shown that medial premotorprojections to the striatum are characterized as a set of distinctcircuits conveying different type of information. This studyassesses the anatomical projections from the supplementary motorarea (SMA), pre-SMA and motor cortex (MC) to the human striatumusing diffusion tensor imaging (DTI) axonal tracking. Eightright-handed volunteers were studied at 1.5 T using DTI axonaltracking. A connectivity matrix was computed, which tested forconnections between cortical areas (MC, SMA and pre-SMA) andsubcortical areas (posterior, middle and anterior putamen andthe head of the caudate nucleus) in each hemisphere. Pre-SMAprojections to the striatum were located rostral to SMA projectionsto the striatum. The SMA and the MC were similarly connectedto the posterior and middle putamen and not to the anteriorstriatum. These data show that the MC and SMA have connectionswith similar parts of the sensorimotor compartment of the humanstriatum, whereas the pre-SMA sends connections to more rostralparts of the striatum, including the associative compartment.     

Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit

OBJECTIVE: This study, which aimed to confirm or invalidate the somatotopic organization of the supplementary motor area (SMA), correlates the pattern of clinical symptoms observed after SMA removal with the extent of resection. METHODS: Eleven patients with medial precentral glioma underwent partial or complete tumoral resection of the SMA. Seven patients underwent preoperative functional magnetic resonance imaging that incorporated speech and motor tasks. During the operation, the primary motor and speech areas and pathways (in the dominant side) were identified by use of intraoperative direct cortical or subcortical stimulation, and these areas were respected. RESULTS: SMA resection resulted in motor deficits, language deficits, or both; the deficits were always regressive, and they corresponded to the SMA syndrome. The topography and severity of these deficits were correlated to the extent of the SMA resection. The location of the deficit corresponded to SMA somatotopy: the representations of the lower limb, the upper limb, the face, and language (in the left-dominant SMA) were located from posterior to anterior. This somatotopy was also observed with functional magnetic resonance imaging. CONCLUSION: Correlation between clinical patterns of deficit and the extent of SMA resection, guided by means of pre- and intraoperative functional methods, provides strong arguments in favor of somatotopy in this area. This knowledge should allow clinicians to base preoperative predictions of the pattern of postsurgical deficit and recovery on the planned resection, thus allowing them to inform patients accurately before the procedure.     

The supplementary motor area syndrome: a neurosurgical review

The supplementary motor area (SMA) syndrome is a frequently encountered clinical phenomenon associated with surgery of the dorsomedial prefrontal lobe. The region has a known motor sequencing function and the dominant pre-SMA specifically is associated with more complex language functions; the SMA is furthermore incorporated in the negative motor network. The SMA has a rich interconnectivity with other cortical regions and subcortical structures using the frontal aslant tract (FAT) and the frontostriatal tract (FST). The development of the SMA syndrome is positively correlated with the extent of resection of the SMA region, especially its medial side. This may be due to interruption of the nearby callosal association fibres as the contralateral SMA has a particular important function in brain plasticity after SMA surgery. The syndrome is characterized by a profound decrease in interhemispheric connectivity of the motor network hubs. Clinical improvement is related to increasing connectivity between the contralateral SMA region and the ipsilateral motor hubs. Overall, most patients know a full recovery of the SMA syndrome, however a minority of patients might continue to suffer from mild motor and speech dysfunction. Rarely, no recovery of neurological function after SMA region resection is reported.

     

Clinical features and significance of negative motor response in intraoperative language mapping during awake craniotomy

The negative motor area and anterior and posterior language areas were localized by intraoperative electrical cortical stimulation under the awake condition to evaluate the clinical significance of these areas. Thirty-seven awake craniotomies with language mapping were performed in 36 patients with brain tumors. The negative motor area was determined in 17 cases, and the anterior and posterior language areas were found in 12 and 6 cases, respectively. The negative motor area was located in the precentral gyrus inferior to the orofacial motor area in 16 cases, and in the inferior frontal gyrus anterior to the orofacial motor area in one case. Both the negative motor area and the anterior language area were determined in 8 cases. Anterior language areas in these 8 cases were located anterior and/or inferior to the negative motor areas. The negative motor area is an easily determined, important landmark for intraoperative language mapping.     

Single-neuron activity in the human supplementary motor area underlying preparation for action

OBJECT: The supplementary motor area (SMA) is considered critical in the planning, initiation, and execution of motor acts. Despite decades of research, including electrical stimulation mapping in patients undergoing neurosurgery, the contribution of this region to the generation of motor behavior has remained enigmatic. This is a study of single-neuron responses at various stages of a motor task during depth electrode recording in the SMA, pre-SMA, and medial temporal lobe of humans, with the goal of elucidating the disparate roles of neurons in these regions during movements. METHODS: The patients were undergoing evaluation for epilepsy surgery requiring implantation of intracranial depth electrodes. Single-unit recordings were made during both the execution and mental imagery of finger apposition sequences. Only medial frontal neurons responded selectively to specific features of the motor plan, such as which hand performed the motor activity or the complexity of the sequence. Neuron activity progressively increased before the patient was given a "go" cue for the execution of movements; this activity peaked earlier in the pre-SMA than in the SMA proper. We observed similar patterns of activation during motor imagery and actual movement, but only neurons in the SMA differentiated between imagined and real movements. CONCLUSIONS: These results provide support at the single-neuron level for the role of the medial frontal cortex in the temporal organization and planning of movements in humans.     

Activation of the supplementary motor area (SMA) during performance of visually guided movements

The supplementary motor area (SMA) has long been thought to have a special role in the internal generation of complex movements. Yet, a number of recent functional imaging studies indicate that the SMA is activated during the execution of simple movements guided by sensory cues. The extent of participation of the cingulate motor areas in visually guided movements also is unclear. To explore these issues we used the 2-deoxyglucose (2DG) technique to measure functional activation in the motor areas on the medial wall of the hemisphere in monkeys trained to perform visually guided reaching movements to randomly presented targets. This approach enabled us to make precise comparisons between sites of activation and the location of specific premotor areas on the medial wall of the hemisphere. We found that the SMA was strongly activated during reaching to different visual targets. Indeed, its activation was comparable to that of the primary motor cortex (M1). In contrast, none of the cingulate motor areas displayed significantly increased activation specifically related to arm movements. Our results provide further support for the involvement of the SMA in visually guided movements. Furthermore, our observations suggest that during externally guided reaching, SMA activation is tightly coupled to that of M1, but dissociated from that of the cingulate motor areas.     

Preoperative mapping of the supplementary motor area in patients harboring tumors in the medial frontal lobe

OBJECT: Injury to the supplementary motor area (SMA) is thought to be responsible for transient motor and speech deficits following resection of tumors involving the medial frontal lobe. Because direct intraoperative localization of SMA is difficult, the authors hypothesized that functional magnetic resonance (fMR) imaging might be useful in predicting the risk of postoperative deficits in patients who undergo resection of tumors in this region. METHODS: Twelve patients who had undergone fMR imaging mapping while performing speech and motor tasks prior to excision of their tumor, that is, based on anatomical landmarks involving the SMA, were included in this study. The distance between the edge of the tumor and the center of SMA activation was measured and was correlated with the risk of incurring postoperative neurological deficits. In every patient, SMA activation was noted in the superior frontal gyrus on preoperative fMR imaging. Two speech and two motor deficits typical of SMA injury were observed in three of the 12 patients. The two speech deficits occurred in patients with tumors involving the dominant hemisphere, whereas one of the motor deficits occurred in a patient with a tumor in the nondominant hemisphere. The risk of developing a postoperative speech or motor deficit was 100% when the distance between the SMA and the tumor was 5 mm or less. When the distance between SMA activation and the lesion was greater than 5 mm, the risk of developing a motor or a speech deficit was 0% (p = 0.0007). CONCLUSIONS: Early data from this study indicated that fMR imaging might be useful in localizing the SMA and in determining the risk of postoperative deficits in patients who undergo resection of tumors located in the medial frontal lobe.     

Frontal and parietal lobe activation during transitive inference in humans

Cortical areas engaged in knowledge manipulation during reasoning were identified with functional magnetic resonance imaging (MRI) while participants performed transitive inference (TI) on an ordered list of 11 items (e.g. if A < B and B < C, then A < C). Initially, participants learned a list of arbitrarily ordered visual shapes. Learning occurred by exposure to pairs of list items that were adjacent in the sequence. Subsequently, functional MR images were acquired as participants performed TI on non-adjacent sequence items. Control tasks consisted of height comparisons (HT) and passive viewing (VIS). Comparison of the TI task with the HT task identified activation resulting from TI, termed 'reasoning', while controlling for rule application, decision processes, perception, and movement, collectively termed 'support processes'. The HT-VIS comparison revealed activation related to support processes. The TI reasoning network included bilateral prefrontal cortex (PFC), pre-supplementary motor area (preSMA), premotor area (PMA), insula, precuneus, and lateral posterior parietal cortex. By contrast, cortical regions activated by support processes included the bilateral supplementary motor area (SMA), primary motor cortex (M1), somatic sensory cortices, and right PMA. These results emphasize the role of a prefrontal-parietal network in manipulating information to form new knowledge based on familiar facts. The findings also demonstrate PFC activation beyond short-term memory to include mental operations associated with reasoning.     

Postoperative deficits and functional recovery following removal of tumors involving the dominant hemisphere supplementary motor area

The supplementary motor area (SMA) is a region located within each cerebral hemisphere at the posterior mesial border of the frontal lobe adjacent to the falx. The functional significance of this area has been somewhat unclear, and information regarding its influence on motor output has largely been based on evoked responses to direct stimulation in primates and humans. In this series of patients with primary and metastatic tumors involving the dominant hemisphere SMA, a distinct pattern of postoperative deficits and recovery has emerged which emphasizes the role of this critical area in the initiation of motor activity, including speech. Based upon this analysis, ablation of this region after first identifying the primary motor cortex may be accomplished without risk of permanent loss of motor activity or speech function, despite the initial severe deficits.     

Cortical connections of the inferior parietal cortical convexity of the macaque monkey

We traced the cortical connections of the 4 cytoarchitectonic fields--Opt, PG, PFG, PF--forming the cortical convexity of the macaque inferior parietal lobule (IPL). Each of these fields displayed markedly distinct sets of connections. Although Opt and PG are both targets of dorsal visual stream and temporal visual areas, PG is also target of somatosensory and auditory areas. Primary parietal and frontal connections of Opt include area PGm and eye-related areas. In contrast, major parietal and frontal connections of PG include IPL, caudal superior parietal lobule (SPL), and agranular frontal arm-related areas. PFG is target of somatosensory areas and also of the medial superior temporal area (MST) and temporal visual areas and is connected with IPL, rostral SPL, and ventral premotor arm- and face-related areas. Finally, PF is primarily connected with somatosensory areas and with parietal and frontal face- and arm-related areas. The present data challenge the bipartite subdivision of the IPL convexity into a caudal and a rostral area (7a and 7b, respectively) and provide a new anatomical frame of reference of the macaque IPL convexity that advances our present knowledge on the functional organization of this cortical sector, giving new insight into its possible role in space perception and motor control.     

Cortical Networks for Visual Reaching: Physiological and Anatomical Organization of Frontal and Parietal Lobe Arm Regions

The functional and structural properties of the dorsolateralfrontal lobe and posterior parietal proximal arm representationswere studied in macaque monkeys. Physiological mapping of primarymotor (MI), dorsal premotor (PMd), and posterior parietal (area5) cortices was performed in behaving monkeys trained in aninstructed-delay reaching task. The parietofrontal corticocorticatconnectivities of these same areas were subsequently examinedanatomically by means of retrograde tracing techniques. Signal-, set-, movement-, and position-related directional neuronalactivities were distributed nonuniformly within the task-relatedareas in both frontal and parietal cortices. Within the frontallobe, moving caudally from PMd to the MI, the activity thatsignals for the visuospatial events leading to target localizationdecreased, while the activity more directly linked to movementgeneration increased. Physiological recordings in the superior parietal lobule revealeda gradient-like distribution of functional properties similarto that observed in the frontal lobe. Signal- and set-relatedactivities were encountered more frequently in the intermediateand ventral part of the medial bank of the intraparietal sulcus(IPS), in area MIP. Movement- and position-related activitieswere distributed more uniformly within the superior parietallobule (SPL), in both dorsal area 5 and in MIP. Frontal and parietal regions sharing similar functional propertieswere preferentially connected through their association pathways.As a result of this study, area MIP, and possibly areas MDPand 7m as well, emerge as the parietal nodes by which visualinformation may be relayed to the frontal lobe arm region. Theseparietal and frontal areas, along with their association connections,represent a potential cortical network for visual reaching.The architecture of this network is ideal for coding reachingas the result of a combination between visual and somatic information.     

Connectivity-based subdivisions of the human right "temporoparietal junction area": evidence for different areas participating in different cortical networks

Controversy surrounds the role of the temporoparietal junction (TPJ) area of the human brain. Although TPJ has been implicated both in reorienting of attention and social cognition, it is still unclear whether these functions have the same neural basis. Indeed, whether TPJ is a precisely identifiable cortical region or a cluster of subregions with separate functions is still a matter of debate. Here, we examined the structural and functional connectivity of TPJ, testing whether TPJ is a unitary area with a heterogeneous functional connectivity profile or a conglomerate of regions with distinctive connectivity. Diffusion-weighted imaging tractrography-based parcellation identified 3 separate regions in TPJ. Resting-state functional connectivity was then used to establish which cortical networks each of these subregions participates in. A dorsal cluster in the middle part of the inferior parietal lobule showed resting-state functional connectivity with, among other areas, lateral anterior prefrontal cortex. Ventrally, an anterior TPJ cluster interacted with ventral prefrontal cortex and anterior insula, while a posterior TPJ cluster interacted with posterior cingulate, temporal pole, and anterior medial prefrontal cortex. These results indicate that TPJ can be subdivided into subregions on the basis of its structural and functional connectivity.     

Cortical connections of area V4 in the macaque

To determine the locus, full extent, and topographic organization of cortical connections of area V4 (visual area 4), we injected anterograde and retrograde tracers under electrophysiological guidance into 21 sites in 9 macaques. Injection sites included representations ranging from central to far peripheral eccentricities in the upper and lower fields. Our results indicated that all parts of V4 are connected with occipital areas V2 (visual area 2), V3 (visual area 3), and V3A (visual complex V3, part A), superior temporal areas V4t (V4 transition zone), MT (medial temporal area), and FST (fundus of the superior temporal sulcus [STS] area), inferior temporal areas TEO (cytoarchitectonic area TEO in posterior inferior temporal cortex) and TE (cytoarchitectonic area TE in anterior temporal cortex), and the frontal eye field (FEF). By contrast, mainly peripheral field representations of V4 are connected with occipitoparietal areas DP (dorsal prelunate area), VIP (ventral intraparietal area), LIP (lateral intraparietal area), PIP (posterior intraparietal area), parieto-occipital area, and MST (medial STS area), and parahippocampal area TF (cytoarchitectonic area TF on the parahippocampal gyrus). Based on the distribution of labeled cells and terminals, projections from V4 to V2 and V3 are feedback, those to V3A, V4t, MT, DP, VIP, PIP, and FEF are the intermediate type, and those to FST, MST, LIP, TEO, TE, and TF are feedforward. Peripheral field projections from V4 to parietal areas could provide a direct route for rapid activation of circuits serving spatial vision and spatial attention. By contrast, the predominance of central field projections from V4 to inferior temporal areas is consistent with the need for detailed form analysis for object vision.     

累及补充运动区额上回胶质瘤的外科治疗

目的　探讨累及补充运动区额上回胶质瘤的外科治疗。方法　对 16例累及补充运动区的低级别星形细胞瘤患者的临床资料及随访结果进行分析。结果　手术切除范围距中央前沟 >1cm的病变 8例 ,其中 6例表现为补充运动区综合征 ,虽出现暂时的运动和语言功能障碍 ,但随访 12个月 ,均得到恢复 ;而手术切除范围距中央前沟 <1cm的 8例病变 ,术后均立即出现对侧肢体偏瘫 ,随访 12个月 ,仍有 5例遗留运动障碍。结论　对于累及补充运动区的额上回胶质瘤 ,当手术切除范围距中央前沟 <1cm时 ,很可能造成永久性的功能障碍     

Postoperative transient hemiplegia after resection of the medial frontal tumor involving the supplementary motor area: report of two cases

The supplementary motor cortex (SMA) is located anterior to the primary motor cortex, and is considered to play an important role in planning, initiating and maintaining sequential motor actions. Disturbance of this area sometimes causes severe contralateral hemiplegia. If the disturbance doesn't affect the primary motor cortex, motor function will recover in relatively early postoperative time. We encountered two cases in which the patients developed postoperative severe hemiplegia after resection of a medial frontal lobe glioma, although there was no apparent change shown in the monitoring of intraoperative motor evoked potential (MEP). Both cases recovered from hemiplegia in the early postoperative period. In our cases, the disturbances of SMA were considered to be the causes of the development of transient hemiplegia. Intraoperative MEP monitoring is useful to distinguish the damage of the primary motor area from that of the SMA.     

When that tune runs through your head: a PET investigation of auditory imagery for familiar melodies.

The present study used positron emission tomography (PET) to examine the cerebral activity pattern associated with auditory imagery for familiar tunes. Subjects either imagined the continuation of nonverbal tunes cued by their first few notes, listened to a short sequence of notes as a control task, or listened and then reimagined that short sequence. Subtraction of the activation in the control task from that in the real-tune imagery task revealed primarily right-sided activation in frontal and superior temporal regions, plus supplementary motor area (SMA). Isolating retrieval of the real tunes by subtracting activation in the reimagine task from that in the real-tune imagery task revealed activation primarily in right frontal areas and right superior temporal gyrus. Subtraction of activation in the control condition from that in the reimagine condition, intended to capture imagery of unfamiliar sequences, revealed activation in SMA, plus some left frontal regions. We conclude that areas of right auditory association cortex, together with right and left frontal cortices, are implicated in imagery for familiar tunes, in accord with previous behavioral, lesion and PET data. Retrieval from musical semantic memory is mediated by structures in the right frontal lobe, in contrast to results from previous studies implicating left frontal areas for all semantic retrieval. The SMA seems to be involved specifically in image generation, implicating a motor code in this process.