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fMRI for preoperative neurosurgical mapping of motor cortex and language in a clinical setting.

PURPOSE: Identification of the precentral gyrus can be difficult in patients with brain tumors. The purpose of the current study was to evaluate the clinical usefulness of functional MRI (fMRI) in identifying motor cortex and speech areas as a part of preoperative neurosurgical planning. METHOD: fMRI was performed using a 1.5 T MR unit in 41 patients with brain tumors. The motor paradigm was finger tapping and foot movement, whereas the language paradigm consisted of a two word semantic test. Statistical analysis of the data was done using the Kolmogorow-Smirnow test. Plots of signal intensities over time were created. RESULTS: The precentral gyrus was identified in 38 of 41 patients. In two patients, fMRI was not of acceptable quality due to motion artifacts. Speech areas were localized in 33 patients. In a typical clinical setting, the value of the method was graded "high." CONCLUSION: fMRI's efficacy in the preoperative localization of language and motor areas is high. The method should become a routine adjunct for preoperative evaluation of brain tumors in the near future.

Adult↗

Differential connections by intracortical axon collaterals among pyramidal tract cells in the cat motor cortex.

1. Recurrent EPSPs were produced in fast pyramidal tract (PT) cells in the cat motor cortex by stimulation of the medullary pyramid and/or by the glutamate-induced activity of neighbouring PT cells using the spike-triggered averaging (spike-TA) method. 2. In fast PT cells located lateral to the end of the cruciate sulcus, predominantly the motor cortical representation area of the distal forelimb, two components (fast and slow) of recurrent EPSPs were produced by pyramid stimulation. 3. In response to pyramid stimulation, the appearance of the fast and slow components of recurrent EPSPs correlated with the appearance of N1 and N2 field potentials, respectively. 4. The monosynaptic nature of both the fast and slow components of recurrent EPSPs was demonstrated by a double shock test (interstimulus interval less than 5 ms) and high frequency repetitive stimulation (50-100 Hz). 5. The generation of the fast and slow components of recurrent EPSPs was attributed to the synaptic action of recurrent collaterals of fast and slow PT cells, respectively. 6. The amplitude of the slow component of recurrent EPSPs markedly increased with an increase in the stimulus frequency whereas that of the fast component did not, despite the change in stimulus frequency. 7. Selected spike-triggered averaging also revealed frequency facilitation of recurrent individual EPSPs produced in fast PT cells by the activity of single slow PT cells. 8. In fast PT cells located in the anterior and posterior lips of the cruciate sulcus, the motor cortical representation area of the proximal limb or trunk, only the slow component of recurrent EPSPs was produced by pyramid stimulation. 9. It is concluded that the pattern of recurrent connections between neighbouring PT cells differs depending on the motor cortical representation area, and that frequency facilitation of recurrent EPSPs is caused mainly by the input from axon collaterals of slow PT cells.

Animals↗

Demonstration of the corticotectobulbar pathway from the orofacial motor cortex to the parvicellular reticular formation in the rat.

We examined a corticotectobulbar pathway from the orofacial motor cortex (OfM) to the parvicellular reticular formation (RFp), where numerous premotor neurons for the orofacial motor nuclei were known to be distributed, light and electron microscopically by using a combination of anterograde and retrograde tracing techniques. After contralateral injections of biotinylated dextranamine (BDA) into the OfM and cholera toxin B subunit (CTb) into the RFp, the overlapping distribution of ipsilateral axon terminals labeled with BDA and contralateral neurons labeled with CTb was found in the lateralmost part of the superior colliculus (SC). Furthermore, contralateral injections of BDA into the OfM and wheat germ agglutinin-horseradish peroxidase (WGA-HRP) into the RFp resulted in that ipsilateral axons labeled with BDA made asymmetrical synaptic contacts with the dendrites of contralateral SC neurons labeled with WGA-HRP.

Animals↗

Gut feelings about recovery after stroke: the organization and reorganization of human swallowing motor cortex.

Swallowing problems can affect as many as one in three patients in the period immediately after a stroke. In some cases this can lead to serious morbidity, in particular malnutrition and pulmonary aspiration. Despite this, swallowing usually recovers completely in the vast majority of patients within weeks. This impressive propensity for recovery is likely to relate to how the area of the motor cortex concerned with swallowing is organized and then reorganized after cerebral injury. Recent studies have indicated that swallowing has a bilateral but asymmetric inter-hemisphere representation within motor and premotor cortex. Damage to the hemisphere that has the greater swallowing output appears to predispose that individual to swallowing problems. However, because there is additional substrate for swallowing in the undamaged hemisphere, the capacity for compensatory reorganization in the contralateral motor cortex might be increased, leading to a greater likelihood of recovery. Swallowing might be an excellent system for studying cortical plasticity, and might prove useful in the development of new therapies aimed at accelerating reorganization in the undamaged hemisphere after unilateral cerebral injury.

Adaptation, Physiological↗

Evolution of specialized pyramidal neurons in primate visual and motor cortex.

The neocortex of primates contains several distinct neuron subtypes. Among these, Betz cells of primary motor cortex and Meynert cells of primary visual cortex are of particular interest for their potential role in specialized sensorimotor adaptations of primates. Betz cells are involved in setting muscle tone prior to fine motor output and Meynert cells participate in the processing of visual motion. We measured the soma volumes of Betz cells, Meynert cells, and adjacent infragranular pyramidal neurons in 23 species of primate and two species of non-primate mammal (Tupaia glis and Pteropus poliocephalus) using unbiased stereological techniques to examine their allometric scaling relationships and socioecological correlations. Results show that Betz somata become proportionally larger with increases in body weight, brain weight, and encephalization whereas Meynert somata remain a constant proportion larger than other visual pyramidal cells. Phylogenetic variance in the volumetric scaling of these neuronal subtypes might be related to species-specific adaptations. Enlargement of Meynert cells in terrestrial anthropoids living in open habitats, for example, might serve as an anatomical substrate for predator detection. Modification of the connectional and physiological properties of these neurons could constitute an important evolutionary mode for species-specific adaptation.

Aged↗

[Effect of high frequency cortical microstimulation on the interhemisphere synchronization in the rat motor cortex].

Long-term posttetanic changes of callosal neurons' synchronisation was studied in the rat motor cortex. Following tetanisation, the synchronisation of previously active cells decreased whereas the cells that became active were mostly synchronised. Ultra "narrow" peaks appeared in callosal interactions and correlated with "intermediate" (30-80 ms) those.

Action Potentials↗

Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat.

Although the corticospinal tract is not essential for the production of the basic locomotor rhythm in cats, it does contribute to the regulation of locomotion, particularly in situations in which there is a requirement for precise control over paw placement or limb trajectory. Lesions of the dorsolateral funiculi at the low thoracic level (T(13)) that completely interrupted both the cortico- and rubrospinal pathways produced long-term deficits in locomotion on a level surface. These deficits included a paw-drag that was probably caused both by a loss of cortico- and rubrospinal input to motoneurones controlling distal muscles as well as by a change in the relative timing of muscles acting around the hip and knee. Smaller lesions produced similar deficits from which the cats recovered relatively quickly. Cats with the largest lesions of the dorsolateral funiculi were unable to modify their gait sufficiently to step over obstacles attached to the treadmill belt even 3-5 months postlesion. These results imply that the medial pathways, the reticulo- and vestibulospinal pathways, are unable to fully compensate for damage to the lateral pathways. Single unit recordings from identified pyramidal tract neurones (PTNs) within the hindlimb representation of the primary motor cortex (area 4) showed that a substantial proportion of neurones (67%) significantly increased their discharge frequency when the cats modified their gait to step over obstacles attached to the treadmill belt. Of those PTNs that showed increased activity during the swing phase, populations of neurones were activated at different times. A large proportion of PTNS discharged early in swing, in phase with knee flexors such as the semitendinosus. Others discharged slightly later, in phase with the activity of ankle flexors, such as tibialis anterior, while still others discharged at the end of swing, in phase with digit dorsiflexors, such as the extensor digitorum brevis. We suggest that different populations of cortical neurones may specifically modify the activity of selected groups of close synergistic muscles during different parts of the swing phase. We further suggest that these modifications are mediated, in part, by groups of interneurones that are involved in determining the base locomotor rhythm. This provides a means by which the changes specified by the descending signal from the motor cortex may be smoothly, and appropriately, incorporated into the locomotor cycle.

Animals↗

[Certain nonlinear properties of motor reactions induced by motor cortex stimulation in the unanesthetized cat].

Nonlinear properties of muscle contraction evoked by macrostimulation of motor cortex were studied in chronic unrestrained cats. Frequency modulated stimulation pulse train was used, the modulation was performed by low frequency (0.2 +/ 10.0 Hz) harmonical signal. Time decrement of the evoked muscle contraction was accompanied by a pronounced increase in its phase lag which reached 20-30 degrees after 3-4 periods of stimulation. The phase lag increase was also observed with diminishing of stimulation intensity. When stimulus intensity varied from 1.7 to 1.2 threshold, the maximal increment of the phase lag reached 30-40 degrees. Possible mechanisms of the observed nonlinear properties of the motor signal transformation are discussed.

Animals↗

Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: An electrophysiological study in the macaque monkey.

To elucidate the functions of nonprimary motor cortical (nPMC) areas whose afferents synapse onto output neurons of the primary motor cortex (PMC), we examined the responses of pyramidal tract neurons (PTNs) and non-PTNs (nPTNs) to electrical stimulation in the three nPMCs, the supplementary motor area (SMA) and the dorsal and ventral divisions of the premotor cortex (PMd and PMv), with extracellular unit recording in alert monkeys. Typical responses of PTNs to nPMC stimulation were early orthodromic excitatory responses followed by inhibitory responses. Among 27 PTNs tested by constructing peri-stimulus time histograms, 19 (70.4%) showed inhibitory responses to stimulation in all of the nPMC areas. In contrast, 5/33 PTNs (15.2%) and 10/72 nPTNs (13.9%) showed excitatory responses to stimulation in all of the nPMCs. The inhibitory responses of PTNs were mediated by inhibitory interneurons, some of which may correspond to nPTNs in the superficial layers of the PMC. These interneurons probably possess widely extended axons and nonspecifically inhibit multiple PTNs in layer V. The excitatory and inhibitory influences, and the patterns of convergence of inputs from the nPMCs onto the PTNs, are important to understand motor control by the nPMC-PMC-spinal cord pathway.

Animals↗

Coherent corticomuscular oscillations originate from primary motor cortex: evidence from patients with early brain lesions.

Coherent oscillations of neurons in the primary motor cortex (M1) have been shown to be involved in the corticospinal control of muscle activity. This interaction between M1 and muscle can be measured by the analysis of corticomuscular coherence in the beta-frequency range (beta-CMCoh; 14-30 Hz). Largely based on magnetoencephalographic (MEG) source-modeling data, it is widely assumed that beta-CMCoh reflects direct coupling between M1 and muscle. Deafferentation is capable of modulating beta-CMCoh, however, and therefore the influence of reafferent somatosensory signaling and corresponding neuronal activity in the somatosensory cortex (S1) has been unclear. We present transcranial magnetic stimulation (TMS) and MEG data from three adult patients suffering from congenital hemiparesis due to pre- and perinatally acquired lesions of the pyramidal tract. In these patients, interhemispheric reorganization had resulted in relocation of M1 to the contralesional hemisphere, ipsilateral to the paretic hand, whereas S1 had remained in the lesioned hemisphere. This topographic dichotomy allowed for an unequivocal topographic differentiation of M1 and S1 with MEG (which is not possible if M1 and S1 are directly adjacent within one hemisphere). In all patients, beta-CMCoh originated from the contralesional M1, in accordance with the TMS-evoked motor responses, and in contrast to the somatosensory evoked fields (SEFs) for which the sources (N20m) were localized in S1 of the lesioned hemisphere. These data provide direct evidence for the concept that beta-CMCoh reflects the motorcortical efferent drive from M1 to the spinal motoneuron pool and muscle. No evidence was found for a relevant contribution of neuronal activity in S1 to beta-CMCoh.

Adult↗

Timing of activity in cerebellar dentate nucleus and cerebral motor cortex during prompt volitional movement.

The discharge of neurons in cerebellar dentate nucleus and cerebral motor cortex was recorded on alternate days in each of 3 monkeys in association with prompt arm movement in response to a light signal. The time of change of the discharge of each neuron in relation to arm movement was computed. The distributions of the time of change for cerebellum and cerebrum overlapped, but the cerebellar distribution was shifted slightly earlier.

Animals↗

Motor cortex involvement in presenile dementia: report of a case.

Alzheimer's disease (AD) is characterized neuropathologically by high densities of neurofibrillary tangles (NFT) and neuritic plaques (NP) in the cerebral cortex, in particular in neocortical association areas and in the hippocampal formation. We report here the case of an AD patient who developed signs of motor dysfunction early in the clinical evolution. A quantitative neuropathologic analysis revealed much higher densities of NFT and NP in the primary motor cortex than is usually observed in AD. This case, together with other reports, points to the existence of neurologically defined subgroups of AD with unusual clinical deficits that are correlated with the regional and laminar distribution of NP and NFT, and further supports the hypothesis that the symptomatology presented by AD patients results from the loss of specific neuronal populations leading to a syndrome of global cortical disconnection.

Aged↗

Consistent features in the forelimb representation of primary motor cortex in rhesus macaques.

The purpose of this study was to systematically map the forelimb area of primary motor cortex (M1) in rhesus macaques in an effort to investigate further the organization of motor output to distal and proximal muscles. We used stimulus-triggered averaging (StTAing) of electromyographic activity to map the cortical representation of 24 simultaneously recorded forelimb muscles. StTAs were obtained by applying 15 microA stimuli to M1 sites while the monkey performed a reach and prehension task. Motor output to body regions other than the forelimb (e.g., face, trunk, and hindlimb) was identified using repetitive intracortical microstimulation to evoke movements. Detailed, muscle-based maps of M1 revealed a central core of distal (wrist, digit, and intrinsic hand) muscle representation surrounded by a "horseshoe"-shaped zone of proximal (shoulder and elbow) muscle representation. The core distal and proximal zones were separated by a relatively large region representing combinations of both distal and proximal muscles. On the basis of its size and characteristics, we argue that this zone is not simply the result of stimulus-current spread, but rather a distinct zone within the forelimb representation containing cells that specify functional synergies of distal and proximal muscles. Electrode tracks extending medially from the medial arm of the proximal muscle representation evoked trunk and hindlimb responses. No distal or proximal muscle poststimulus effects were found in this region. These results argue against the existence of a second, major noncontiguous distal or proximal forelimb representation located medially within the macaque M1 representation.

Animals↗

[Dynamics of functional interconnections between cerebral motor cortex neurons of cats under stimulation].

In acute experiments on cats the activity of the motor cortex neurons was recorded. The dynamics of interneuronal connections at passive bending and electrostimulation of the limb contralateral to the place of recording was studied by methods of cross-correlation analysis of impulse trains. At passive bending a considerable decrease of the number of common inputs between neighbouring neurons (within 50-100 microns) and an increase in their number between remote (from 100 till 400 microns) cortical neurons. During electro-stimulation a certain increase in the number of direct inhibitory interactions between the neighbouring neurons was observed.

Animals↗

Organization of adult motor cortex representation patterns following neonatal forelimb nerve injury in rats.

Somatotopic representation patterns in the motor cortex (MI) of rats that had a unilateral forelimb amputation on the first postnatal day were examined after 2-4 months of survival. Intracortical electrical stimulation and recording techniques were used to map the somatic representation in MI and in the somatic sensory cortex (SI). In normal rats, vibrissa, forelimb, and hindlimb areas comprise the bulk of the MI representation. Stimulation within the forelimb area elicits elbow, wrist, or digit movements at the lowest current intensities. The proximal limb representation appears to be contained within the distal forelimb area, since shoulder movements are nearly always evoked by stimulating at higher current intensities at some distal forelimb sites. In agreement with previous studies, the distal forelimb representation overlapped the adjacent part of the granular SI cortex. Following removal of the forelimb at birth, 3 novel features of MI organization were observed. First, the areas from which stimulation evoked movements of the vibrissa or the shoulder musculature were larger than normal. Stimulation thresholds were lower than those required for comparable movements in normal rats throughout these areas, suggesting that nerve section had not simply unmasked a high-threshold representation. Second, vibrissa movements were more commonly paired with movements of the proximal forelimb muscles at the same site. Third, stimulation in the adjacent granular SI cortex failed to evoke shoulder or trunk movements, although receptive-field mapping in this region showed that cells were responsive to cutaneous stimulation of the trunk and shoulder region. These results indicate that several organizational features develop differently in MI following perinatal nerve injury: certain remaining muscle groups have enlarged cortical representations, there is a strengthening of some normally weak connections from MI to the proximal musculature, and muscles are grouped in unusual combinations. These data demonstrate that the formation of MI representation patterns is strongly influenced by nerve injury during the perinatal period.

Amputation, Surgical↗

Activity of different classes of neurons of the motor cortex during locomotion.

This study examines the activity of different classes of neurons of the motor cortex in the rabbit during two locomotion tasks: a simple (on a flat surface) and a complex (overstepping a series of barriers) locomotion. Four classes of efferent neurons were studied: corticocortical (CC) neurons with ipsilateral projection (CCIs), those with contralateral projection (CCCs), descending corticofugal neurons of layer V (CF5s), and those of layer VI (CF6s). In addition, one class of inhibitory interneurons (SINs) was investigated. CF5 neurons and SINs were the only groups that were strongly active during locomotion. In most of these neurons a clear-cut modulation of discharge in the locomotion rhythm was observed. During simple locomotion, CF5s and SINs were preferentially active in opposite phases of the step cycle, suggesting that SINs contribute to formation of the step-related pattern of CF5s. Transition from simple to complex locomotion was associated with changes of the discharge pattern of the majority of CF5 neurons and SINs. In contrast to CF5 neurons, other classes of efferent neurons (CCI, CCC, CF6) were much less active during both simple and complex locomotion. That suggests that CC interactions, both within a hemisphere (mediated by CCIs) and between hemispheres (mediated by CCCs), as well as corticothalamic interactions via CF6 neurons are not essential for motor coordination during either simple or complex locomotion tasks.

Action Potentials↗

Chronic motor cortex stimulation for phantom limb pain: correlations between pain relief and functional imaging studies.

Chronic motor cortex stimulation (CMCS) has provided satisfactory control of pain in patients with central or trigeminal neuropathic pain. We used this technique in 3 patients with intractable phantom limb pain after upper limb amputation. Functional magnetic resonance imaging (fMRI) correlated to anatomical MRI permitted frameless image guidance for electrode placement. Pain control was obtained for all the patients initially and the relief was stable in 2 of the 3 patients at 2 year follow-up. CMCS can be used to relieve phantom limb pain. fMRI data are useful in assisting the neurosurgeon in electrode placement for this indication.

Adult↗