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Sensory motor cortex: correlation of presurgical mapping with functional MR imaging and invasive cortical mapping.

PURPOSE: To describe a clinically useful application of functional magnetic resonance (MR) imaging--presurgical mapping of the sensory motor cortex--and to validate the results with established physiologic techniques. MATERIALS AND METHODS: Functional MR mapping of the sensory motor cortex was performed in two women, aged 24 and 38 years. Both had intractable, simple partial motor seizures due to tumors located in or near the sensory motor cortex. They subsequently underwent invasive cortical mapping--direct cortical stimulation and/or sensory-evoked-potential recording--to localize the affected sensory motor area prior to tumor resection. RESULTS: In both patients, the functional MR study demonstrated task activation of the sensory motor cortex. In both cases, results of cortical functional mapping with invasive techniques matched those obtained with functional MR imaging. CONCLUSION: Presurgical mapping of the sensory motor cortex is a potentially useful clinical application of functional MR imaging.

Adult↗

Intrinsic synaptic organization of the motor cortex.

Recent anatomical and electrophysiological studies of the intrinsic synaptic circuitry of the motor cortex are revealing novel aspects related to the functional organization of this cortical area. These studies demonstrate that the motor cortex is composed of modules consisting of columnar aggregates of neurons related to different aspects of the same movement. Excitatory and inhibitory connections of intracortical origin link neurons within each of these cortical modules, and also mediate interactions between different cortical modules located as far as 2-3 mm from each other. The intrinsic excitatory connections utilize glutamate, and act via both NMDA and non-NMDA postsynaptic receptors. The intrinsic inhibitory connections are GABAergic. Intrinsic cortical circuits are involved in the temporal coordination of different cortical modules for the execution of complex movement patterns. In addition, the intrinsic inhibitory and excitatory connections are involved in the plasticity of representation zones in the motor cortex, a phenomenon that occurs following nerve damage or during the acquisition of novel motor skills.

Animals↗

Using extirpations to understand the human motor cortex: Horsley, Foerster, and Bucy.

During the last part of the 19th century and through the middle of the 20th century, surgeons sometimes extirpated parts of the human motor cortex to control abnormal involuntary movements. This procedure can be traced directly to Victor Horsley, who pioneered the first successful surgery of this type in 1886. Although many neurosurgeons followed Horsley's lead in performing this procedure, few used their results, as he did, to formulate concepts on the role of the motor cortex in movement control. Otfrid Foerster and Paul Bucy were the principal exceptions. We reviewed the surgical procedures these 3 notable neurosurgeons performed on the motor cortex and the hypotheses they subsequently developed on the functions of the motor cortex. We also evaluated these writings relative to contemporary views of motor cortex function.

England↗

Corticocortical connections to the motor cortex from the posterior parietal lobe (areas 5a, 5b, 7) in the cat demonstrated by the retrograde axonal transport of horseradish peroxidase.

Neurons in the parietal region of the cerebral cortex, projecting to the ipsilateral distal forelimb area of the motor cortex (area 4 gamma) were identified in the cat brain using the horseradish peroxidase (HRP) retrograde tracing method. After making microinjections of HRP into the distal forelimb area of the motor cortex, clusters of HRP-labeled cell bodies were observed in different regions of the ipsilateral parietal cortex. In particular these clusters of labeled cells were found in areas 5a, 5b and 7. The area 5a cluster is formed from closely packed irregularly-shaped cells, the area 5b cluster is made up of dispersed medium-sized pyramidal cells, while area 7 contains a cluster of widely dispersed small pyramidal cells. Typically, labeled cell bodies were found in lamina III of cortex. Labeled cell bodies were neither observed in the contralateral cortex nor in the visual cortex (areas 17, 18 and 19). Since parietal cortex receives projections from primary somatosensory and visual cortex, the projections from parietal to motor cortex may well form the neural substrate for the processing of convergent sensory information used in voluntary movements.

Afferent Pathways↗

Convergence of limbic input to the cingulate motor cortex in the rhesus monkey.

Limbic system influences on motor behavior seem widespread, and could range from the initiation of action to the motivational pace of motor output. Motor abnormalities are also a common feature of psychiatric illness. Several subcortical limbic-motor entry points have been defined in recent years, but cortical entry points are understood poorly, despite the fact that a part of the limbic lobe, the cingulate motor cortex (area 24c or M3, and area 23c or M4), contributes axons to the corticospinal pathway. Using retrograde and anterograde tracers in rhesus monkeys, we investigated the ipsilateral limbic input to area 24c and adjacent area 23c. Limbic cortical input to areas 24c and 23c arise from cingulate areas 24a, 24b, 23a, 23b, and 32, retrosplenial areas 30 and 29, and temporal areas 35, TF and TH. Areas 24c and 23c were also interconnected strongly. The dysgranular part of the orbitofrontal cortex and insula projects primarily to area 24c while the granular part of the orbitofrontal cortex and insula projects primarily to area 23c. Afferents from cingulate area 25, the retrocalcarine cortex, temporal pole, entorhinal cortex, parasubiculum, and the medial part of area TH target primarily or only area 24c. Our findings indicate that a variety of telencephalic limbic afferents converge on cortex lining the lower bank and fundus of the anterior part of the cingulate sulcus. Because it is known that this cortex gives rise to axons ending in the spinal cord, facial nucleus, pontine gray, red nucleus, putamen, and primary and supplementary motor cortices, we suggest that the cingulate motor cortex forms a strategic cortical entry point for limbic influence on the voluntary motor system.

Amino Acids↗

Linear summation of cat motor cortex outputs.

Recruitment of movement-related muscle synergies involves the functional linking of motor cortical points. We asked how the outputs of two simultaneously stimulated motor cortical points would interact. To this end, experiments were done in ketamine-anesthetized cats. When prolonged (e.g., 500 ms) trains of intracortical microstimulation were applied in the primary motor cortex, stimulus currents as low as 10-20 microA evoked coordinated movements of the contralateral forelimb. Paw kinematics in three dimensions and the electromyographic (EMG) activity of eight muscles were simultaneously recorded. We show that the EMG outputs of two cortical points simultaneously stimulated are additive. The movements were represented as displacement vectors pointing from initial to final paw position. The displacement vectors resulting from simultaneous stimulation of two cortical points pointed in nearly the same direction as the algebraic resultant vector. Linear summation of outputs was also found when inhibition at one of the cortical points was reduced by GABAA receptor antagonists. A simple principle emerges from these results. Notwithstanding the underlying complex neuronal circuitry, motor cortex outputs combine nearly linearly in terms of movement direction and muscle activation patterns. Importantly, simultaneous activation does not change the nature of the output at each point. An additional implication is that not all possible movements need be explicitly represented in the motor cortex; a large number of different movements may be synthesized from a smaller repertoire.

Algorithms↗

[Limited paralysis of the hand caused by metastasis in the motor cortex].

A 66-year old man presented a progressive motor deficit of the left hand mimicking radial and ulnar paralysis. Clinical examination, laboratory investigations, and post mortem findings, demonstrated a single metastasis in the contralateral motor cortex. The interest of this case lies in the discrepancy between the extent of the motor deficit and the size of the lesion. This finding could help to interpret current theories concerning the somatotopic representation on the motor cortex in man.

Aged↗

An investigation of the intrinsic circuitry of the motor cortex of the monkey using intra-cortical microstimulation.

The motor cortex contains a distributed map of muscles, with a single muscle represented over a wide cortical area. We have searched for inter-connections between distant sites projecting to common muscles by delivering pairs of 20-microA single-pulse intracortical microstimuli (ICMS) to sites separated by 1.5-2 mm in the hand-area primary motor cortex of two macaque monkeys performing a precision grip task. The facilitation of hand- and forearm-muscle rectified EMG was measured. When stimuli were delivered simultaneously, responses were quantified using a technique to correct for non-linearities inherent in the use of averaged, rectified EMG. A spatial facilitation was seen for such simultaneous stimuli; however, it was of the same magnitude as that occurring when ICMS was paired with stimulation of corticospinal axons in the pyramidal tract (PT), so that it was likely to be spinal in origin. When two such distant sites were stimulated separated by a 10- or 20-ms delay, the second response scaled with the level of background EMG in the same way as a response to the PT stimulus. By contrast, when the same site was stimulated twice with these delays, the second response showed a facilitation compared with a similarly timed PT response. There would therefore appear to be a local facilitation of the cortical output at these intervals, which is not seen between distant sites. Antidromically identified pyramidal-tract neurones (PTNs) were recorded whilst stimuli were delivered to a cortical site, with a distance between stimulating and recording electrodes of also 1.5-2 mm. The most common response was a facilitation followed by a suppression. Six of eleven PTNs showed a facilitation in their discharge following this stimulation (maximum connection strength s=0.19), 8/11 showed a suppression (maximum s=0.16). It is concluded that powerful inter-connections do exist between distributed parts of the motor output and that there is widespread cortical activation after even a single ICMS pulse. However, these inter-connections do not lead to interactions between cortical outputs following stimulation, as assessed from the EMG. It is proposed that this is likely to reflect differences in the summation of output cells to local versus remote stimulation.

Animals↗

Effect of forelimb use on postnatal development of the forelimb motor representation in primary motor cortex of the cat.

In the cat, the motor representation in motor cortex develops between wk 8 and wk 13. Motor map development is accompanied by a decrease in the current thresholds for evoking movements with a concomitant increase in the number of effective sites, an increase in the distal representation, and the representation of multijoint synergies. In this study we used intracortical microstimulation in anesthetized cats to examine how forelimb motor experiences influence development of map characteristics. To promote skilled movements during wks 8-13, animals were engaged in daily performance of a prehension task. Forelimb movements were prevented by intramuscular botulinum toxin injection or restraint. To determine whether experience-dependent changes were permanent, we examined the map in different animals between 1 wk and 1 yr after cessation of testing. Promoting forelimb use resulted in an increase in the number of sites from which multiple joint effects were produced by stimulation and the number of joints represented at those sites. The effect was maximal at 1 wk after cessation of testing, and became progressively less at 1 mo and at 4 mo. Preventing limb use resulted in a decreased number of effective sites, an increase in current thresholds for evoking responses, and a decreased representation of joints at multijoint sites. Our findings show that the motor map can respond to novel motor demands as it is forming during development but that it reverts back to one with the properties of a map in a control animal if those demands are not maintained in the animal's behavioral repertoire.

Age Factors↗

Low threshold unilateral and bilateral facial movements evoked by motor cortex stimulation in cats.

Organizational features of the ipsilateral representation in the cat face motor cortex were investigated by using the technique of intracortical microstimulation (less than 30 microA). In 4 intact animals, 61 efferent zones controlling facial muscles were identified. They were devoted to contralateral muscles (contralateral efferent zones; n = 35), ipsilateral muscles (ipsilateral efferent zones; n = 8) or symmetrical muscles of both sides (bilateral efferent zones; n = 18). Contralateral efferent zones were found within both the rostral part of the coronal gyrus and the lateral bank of the presylvian sulcus, whereas ipsilateral and bilateral efferent zones were exclusively localized to the rostromedial region of the face motor cortex. Movement thresholds proved to be lowest at the contralateral efferent zones and highest at the ipsilateral efferent zones, with intermediate values at the bilateral efferent zones. Latencies of suprathreshold EMG responses evoked from contralateral and ipsilateral efferent zones were the shortest and the longest, respectively; intermediate values were found upon stimulation of sites from bilateral efferent zones. The efferent zones identified in 3 lesioned animals (two cats with contralateral motor cortex ablation and one cat with transection of the rostral two thirds of the corpus callosum) were contralateral (n = 14), bilateral (n = 13), and ipsilateral (n = 9). Mean thresholds of effective sites from bilateral and ipsilateral efferent zones in lesioned preparations were not significantly higher than those in intact animals. This would thus suggest that extracallosal pathways may account for ipsilateral responses.

Animals↗

Transcranial electrical stimulation of the motor cortex in man: further evidence for the site of activation.

1. The motor cortex was stimulated electrically (vertex anode; cathode 6 cm lateral) in neurologically normal subjects undergoing surgery for scoliosis, and the evoked corticospinal volleys were recorded from the spinal cord using epidural electrodes. 2. Stimuli > 330 V produced a complex D-wave volley containing three separate peaks, with high-threshold components, 0.8 ms (D2) and 1.6 ms (D3), in advance of the lowest-threshold component (D1). As stimuli increased up to 1500 V, D3 replaced the later components completely, but there was no further latency 'jump'. 3. Brainstem stimulation using electrodes over each mastoid process produced a descending volley that had the same latencies as D3. At threshold, stimulation of the brainstem or spinal cord attenuated the D wave evoked by simultaneous cortical stimulation. 4. It is concluded that transcranial electrical stimulation of the motor cortex at high intensities can access corticospinal neurones at the pyramidal decussation, and that stimulation of the brainstem (and the spinal cord) preferentially accesses corticospinal axons. At threshold, motor cortex stimulation probably activates corticospinal neurones at or near the cerebral cortex.

Adolescent↗

Excitability of the motor cortex to magnetic stimulation in patients with cerebellar lesions.

The excitability of the motor cortex to magnetic stimulation was evaluated in seven patients with cerebellar lesions (six patients with a unilateral lesion) and in 20 control subjects. Magnetic motor threshold was defined at rest. In all but one of the patients with a hemicerebellar lesion the threshold was higher in the motor cortex contralateral to the impaired hemicerebellum and the right/left threshold asymmetry was clearly greater than normal. In the patient with a lesion involving both cerebellar hemispheres the magnetic threshold was above the normal limit on both sides. The latencies of motor responses were normal in all patients. This increase in the magnetic threshold of the motor cortex functionally related to the impaired hemicerebellum suggests the existence of a facilitating tonic action of the cerebellum on central motor circuits that might act at the cortical, or spinal level, or both.

Adult↗

Hand motor cortex activation in a patient with congenital mirror movements: a study of the silent period following focal transcranial magnetic stimulation.

Motor evoked potentials (MEPs) to focal transcranial magnetic stimulation (TMS) have demonstrated that abnormal ipsilateral corticospinal projections are active in patients with congenital mirror movements. In addition, movement-related potentials and PET suggest that an abnormal pattern of motor cortex activation could be associated with an anomaly of the corticospinal tracts. In the present study the silent period (SP) following focal TMS was investigated in a woman with familial congenital mirror movements. Recordings were made from both abductor pollicis brevis (APB) muscles. When focal TMS was delivered during an intended contralateral APB muscle contraction, MEP and SP were bilaterally recorded and SP was significantly shorter than the contralateral SP observed in normal controls. An abnormal bilateral activation of the hand motor cortex can explain our findings. The non-stimulated motor cortex causes an early partial recovery of the background EMG activity when the stimulated motor cortex is still inhibited (beginning as soon as the transcallosal and the short-lasting segmental inhibition are both complete).

Adult↗

Current density threshold for the stimulation of neurons in the motor cortex area.

The aim of this study was to determine a current density threshold for exciting the motor cortex area of the brain. The current density threshold for excitation of nerve fibres (20 microm in diameter) found in the literature is approximately 1 A/m(2) at frequencies lower than 1 kHz. In consideration of a safety factor of 100, the International Commission on Non-Ionizing Radiation Protection (ICNIRP) recommends to restrict the exposure to 0.01 A/m(2). The electromagnetic stimulation of neurons in the motor cortex is used in the clinical diagnosis of nerve lesions and neuropathy by means of magnetic or electrical transcranial stimulation. Combining medical data from clinical studies and technical specifications of the Magstim Model 200 stimulator, we were able to compute the current density threshold for the excitation of the human motor cortex by means of the finite element method (FEM). A 3D-CAD head model was built on the basis of magnetic resonance imaging (MRI) slices and segmented into four anatomical structures (scalp, skull, brain, and ventricular system) with different conductivities. A current density threshold for the stimulation of the motor cortex area of the upper limbs of 6 and 2.5 A/m(2) at 2.44 kHz and 50 Hz, respectively, was calculated. As these values lie above the recommended ICNIRP values by two orders of magnitude there is no need for lower safety standards with regard to stimulation of the brain.

Central Nervous System Diseases↗

Experiments on functional role of peripheral input to motor cortex during voluntary movements in the monkey.

The functional role of sensory input to the motor cortex was studied by interrupting two major input pathways. One was the dorsal column, which sends the input directly through the thalamus to the motor cortex, and the other was the sensory cortex, which transfers its input through association fibers. Removal of the sensory cortex produced very little motor disturbances and the function recovered within a week. Section of the dorsal column produced some motor deficit, but the deficit was not severe and the animals recovered nearly completely within 2 wk. Combination of dorsal column section and sensory cortex removal produced severe motor deficits. These consisted of loss of orientation within extrapersonal space and loss of dexterity of individual fingers. These deficits never recovered within the duration of observation, which lasted 4-5 wk. It is concluded that the direct sensory input from the thalamus plays an important role in the control of voluntary movements, but loss of its function can be compensated by the input from the sensory cortex. The possible neuronal basis for the observed motor deficits is discussed and it is proposed that the sensory input functions by selectively changing the excitability of cortical efferent zones before and during the execution of voluntary movements. Recovery of motor function following dorsal column section occurred in parallel with the recovery of sensory input to the motor cortex. The recovered function and sensory input disappeared again following section of the association fibers from the sensory cortex. Neuronal mechanism for this observation is also discussed.

Afferent Pathways↗

The role of primary motor cortex in goal-directed movements: insights from neurophysiological studies on non-human primates.

Neurophysiological studies on non-human primates have provided a large body of information on the response patterns of neurons in primary motor cortex during volitional motor tasks. Rather than finding a single simple pattern of activity in primary motor cortex neurons, these studies illustrate that neural activity in this area reflects many different types of information, including spatial goals, hand motion, joint motion, force output and electromyographic activity. This richness in the response characteristics of neurons makes estimates of any single variable on motor performance from population signals imprecise and prone to errors. It initially seems puzzling that so many different types of information are represented in primary motor cortex. However, such richness in neural responses reflects its important role in converting high-level behavioral goals generated in other cortical regions into complex spatiotemporal patterns to control not only alpha-motoneuron activity but also other features of spinal processing.

Animals↗

Role of adaptive plasticity in recovery of function after damage to motor cortex.

Based upon neurophysiologic, neuroanatomic, and neuroimaging studies conducted over the past two decades, the cerebral cortex can now be viewed as functionally and structurally dynamic. More specifically, the functional topography of the motor cortex (commonly called the motor homunculus or motor map), can be modified by a variety of experimental manipulations, including peripheral or central injury, electrical stimulation, pharmacologic treatment, and behavioral experience. The specific types of behavioral experiences that induce long-term plasticity in motor maps appear to be limited to those that entail the development of new motor skills. Moreover, recent evidence demonstrates that functional alterations in motor cortex organization are accompanied by changes in dendritic and synaptic structure, as well as alterations in the regulation of cortical neurotransmitter systems. These findings have strong clinical relevance as it has recently been shown that after injury to the motor cortex, as might occur in stroke, post-injury behavioral experience may play an adaptive role in modifying the functional organization of the remaining, intact cortical tissue.

Adaptation, Physiological↗

Anticipatory activity in primary motor cortex codes memorized movement sequences.

Movement sequences, defined both by the component movements and by the serial order in which they are produced, are fundamental building blocks of motor behavior. The serial order of sequence production is strongly encoded in medial motor areas. It is not known to what extent sequences are further elaborated or encoded in primary motor cortex. Here, we describe cells in the primary motor cortex of the monkey that show anticipatory activity exclusively related to a specific memorized sequence of upcoming movements. In addition, the injection of muscimol, a GABA agonist, into motor cortex resulted in an increase in the error rate during sequence production, without concomitant effects on nonsequenced motor performance. Our results challenge the role of medial motor areas in the control of well-practiced movement sequences and suggest that motor cortex contains a complete apparatus for the planning and production of this complex behavior.

Action Potentials↗