(Stroke. 1997;28:110-117.)
© 1997 American Heart Association, Inc.
Articles |
Mapping of Motor Cortical Reorganization After Stroke
A Brain Stimulation Study With Focal Magnetic Pulses
the IRCCS S Lucia (R.T., P.C., A.B., P.M.R., G.B.); Clinica Neurologica, Universita "Tor Vergata," (G.B.); and Ospedale Fatebenefratelli Isola Tiberina, Divisione di Neurologia (P.M.R.), Rome, Italy.
Correspondence to Dr Raimondo Traversa, IRCCS S Lucia, via Ardeatina 306, 00179 Rome, Italy.
 |
Abstract |
|---|
 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Background and Purpose Focal transcranial magnetic stimulation (TCS) is used for noninvasive and painless mapping of the somatotopical organization of the motor cortex. TCS mapping of motor cortical output to the abductor digiti minimi (ADM) muscle was followed up in monohemispheric stroke patients by evaluating motor evoked potentials (MEPs). This approach allowed noninvasive investigation of the functional reorganization of hand motor areas.
Methods Motor maps were constructed for 15 subacute stroke patients about 2 months from the ictus by recording MEPs from the ADM muscle via focal TCS in the affected hemisphere (AH) and unaffected hemisphere (UH) at the beginning of (T1) and after 8 to 10 weeks of neurorehabilitation (T2). Barthel Index and Canadian Neurological Scale scores were evaluated as well. An age-sex matched group of 15 healthy control subjects was enrolled to establish normative data.
Results MEP excitability threshold was significantly higher in the AH of stroke patients than in normal subjects and in the UH (P<.001); excitability threshold was not significantly different between normal subjects and UH. In the AH, MEPs were significantly (P<.001) delayed in latency both in T1 and T2, with a significant decrease of the extenuation of motor output area to the ADM muscle (P<.05) in T1 versus control group and UH. This area was significantly enlarged (P<.05) in T2. Amplitude of MEPs from the AH, both at rest and during voluntary contraction, was significantly lower than normal in T1 (P<.001); it increased in T2 (P<.01) during relaxation but was still smaller than normal during contraction (P<.001). In combination with these findings, an improvement of Barthel Index and Canadian Neurological Scale scores (P<.001) was observed between T1 and T2 (P<.001). Central conduction time was prolonged in stroke patients both in T1 and T2. Changes in the shape of motor maps in the AH during follow-up in T2 were either isolated (therefore increasing the interhemispheric asymmetry) or also were "mirrored" on the UH.
Conclusions Our neurophysiological data are consistent with the presence of a rearrangement of the motor cortical output area and correlate well with an improvement of motor performances. These findings confirm the existence in adults of a "plasticity" in the central nervous system that is still operating between 2 and 4 months from the acute ictal episode. The observed neurophysiological modifications are significantly correlated with clinical improvement of disability and clinical scores.
Key Words: cerebrovascular disorders • motor activity • neuronal plasticity • stroke outcome
|
Introduction |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Transcranial electric and magnetic stimulation of the corticospinal tracts represents a unique noninvasive method for testing impulse propagation along pyramidal fibers.1 2 3 4 5 Absent or severely depressed MEPs after a stroke have been described by several authors, and their usefulness in predicting the final outcome has been suggested.6 7 8 9 10 11 12 13 14 15
Magnetic stimulators able to induce transcranial focal activation of the brain have been successfully used for noninvasive and painless mapping of the somatotopical organization of the motor cortex.16 17 18 19 20 21 This type of analysis has proved to be reliable and reproducible19 and has been used with success in depicting short- and long-term reorganization of the cortical motor output after hemispherectomy,22 spinal cord lesions,23 limb amputation,24 limb and finger transient anesthesia,25 26 and prolonged immobilization.27
In the present study, we aimed to investigate the reorganization of hand motor maps after a vascular monohemispheric lesion by constructing motor maps of representative upper limb muscles with focal TCS. Moreover, the analysis was performed on both unaffected and affected hemispheres and compared with analysis of a group of healthy volunteers. The enrolled patients were evaluated during a neurorehabilitation cycle, with the recording sessions performed at the beginning and during the course of a rehabilitation program. Patients' clinical recovery and hand functionality correlated well with reshaping of motor cortical output during follow-up as tested with TCS.
|
Subjects and Methods |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Fifteen patients affected by stroke (10 men, 5 women; mean age, 62.6 years [range, 30 to 80 years]) entered the study. Criteria for their inclusion were (1) monohemispheric stroke resulting in a relatively stabilized neurological condition (35 to 60 days before enrollment); (2) CT or MRI documenting a monohemispheric unique lesion; (3) age below 80 years; and (4) first-ever attack. Exclusion criteria were concomitant neuropathies, systemic vasculopathies, dementia, or severe aphasia making patients uncooperative. All patients and healthy control subjects provided fully informed consent. The experimental protocol was approved by the local ethics committee.
Eleven and 4 patients suffered left and right hemispheric lesions, respectively. On the basis of CT findings, a lesion was classified as "cortical" if it involved cortical structures and subcortical white matter, excluding basal ganglia and internal capsule, and "subcortical" if there was no visible cortical lesion combined with the involvement of the caudate nucleus, internal capsule, putamen, or globus pallidus.28 According to this subdivision, 7 patients presented as cortical, and the remaining 8 were classified as subcortical (see Table 3
). Because each patient was followed up and, in this early phase of the study, we wanted to test the sensitivity of the method to track the evolution of neurological stroke effects of various severities, no preliminary selection regarding either clinical status or anatomic (CT-MRI) extension of the lesion was carried out. Clinical improvement was evaluated with current standardized scales: Barthel Index for disability29 and Canadian Neurological Scale30 for neurological status; subscoring for hand functionality was extrapolated from the Canadian Neurological Scale (hand motor score). During the hospitalization, all the patients underwent daily rehabilitation treatment based mainly on the Bobath approach.31
|
The first recording session was performed on admission (T1) and the second after 8 to 10 weeks of neurorehabilitation (T2). Before recording sessions, patients underwent a complete neurological examination.
A control population of 15 right-handed subjects (6 men, 9 women; mean age, 58.1 years [range, 31 to 77 years]) was selected. In 4 of them, a second recording session was performed as a "retest" condition to evaluate data reproducibility. Normative data have been extensively detailed elsewhere.32
Stimulation Procedures
Focal TCS was delivered by using a figure-8 coil (double 70-mm coil, Magstim) connected with a Novametrix stimulator (Magstim 200 B). A tightly adherent and transparent nonelastic plastic cap was modeled on the subject's head. Anatomic landmarks (nasion-inion line or sagittal plane, interaural line on coronal plane, ear and meatal profiles) were traced on it to obtain a reproducible topography for mapping the same scalp sites in T2. Eleven positions on each hemiscalp were scanned, covering the precentral area in a scalp district 0 to 8 cm lateral to the sagittal plane and from 1 cm posterior to 8 cm anterior to the coronal plane (Fig 1). A larger number of stimulation positions was avoided to make the test tolerable for patients (total duration around 1 hour). Moreover, a pilot study in normal subjects32 had previously shown that the selected scalp sites were sufficient to fully depict the ADM map of the corticospinal output.
|
Recording Procedures
While subjects were completely relaxed and lying with open eyes on a bed, MEPs were bilaterally recorded from ADM muscles with surface electrodes taped in a belly-tendon montage. Nicolet Spirit recording equipment was used (sensitivity, 125 to 500 µV/division; filters, 2 to 2000 Hz). A ground electrode was placed proximal to the recording sites.
At first, the ET for MEP elicitation was defined according to standardized criteria4 32 33 ; thereafter, the TCS intensity was increased by about 10% to obtain a greater probability of eliciting MEPs. The same TCS intensity as in T1 was also maintained in T2 to reproduce the same conditions in both recording sessions. A cascade of four consecutive MEPs was gathered from each stimulation site, maintaining the optimal coil-axis orientation (approximately perpendicular to the presumed location of the central sulcus20 ) in relaxed awake subjects. At the scalp site where MEPs of maximal amplitude were obtained at rest, MEP recordings were repeated during contraction whenever the patient was able to perform it.
Data Analysis
The following parameters were taken into consideration: (1) ET, (2) analysis of hand motor area extension as represented by the number of responsive sites, (3) analysis of the scalp site from which MEPs of maximal amplitude and minimal latency could be elicited ("hot spot"), (4) MEP amplitude measured peak to peak as triggered during hot-spot TCS during both relaxation and contraction, (5) MEP latency from the hot spot, and (6) CCT obtained via the "F wave" method.2 3 4
Pooled data for each considered parameter were statistically compared with the homologous set of data in the two sessions and/or with the control group via paired Student's t test. Correlation coefficients of neurophysiological parameters versus clinical scores and CT findings were obtained via linear regression. Mean±2 to 3 SDs were used to define abnormality thresholds.
|
Results |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Control Group
Table 1
shows the neurophysiological data for 15 age-matched volunteers. The mean±SD ETs for right and left hemispheres were 48.4±7.5% and 46.4±7.6%, respectively. The mean±SD numbers of scalp sites from which MEPs could be elicited were on average 3.6±1.4 on the right hemisphere and 3.6±2.0 on the left. In 9 subjects, there were more responsive sites on the right hemisphere, and in 4 the predominance was on the left. Optimal MEPs (lowest threshold, maximal amplitude, and shortest latency equal a "hot spot") were recorded after TCS of the hot spot on each hemisphere (see Fig 4). In 12 subjects, a slight asymmetry on the sagittal plane of the hot-spot location was found: in 6 it was more anterior on the left hemisphere, while in 5 the opposite was found. No consistent asymmetries were encountered on the coronal plane.
|
|
MEP amplitude in relaxed condition during hot-spot TCS was 350±122 µV for the right hemisphere and 297±157 µV for the left; amplitudes during contraction were 3418±1237 and 3409±1185 µV, respectively. MEP latency during relaxation was 22.2±1.4 and 22.1±1.1 milliseconds and CCT was 7.7±1.1 and 7.4±1.2 milliseconds for the right and left hemispheres, respectively.
The second recording session ("retest") did not show significant variations in any of the tested parameters. This supported the assumption that the observed changes during follow-up in patients were not due to technical factors or physiological variability of the measured parameters.
Patient Group
Patients completed the recording session without complications; moreover, no adverse side effects were reported during the session or in the following hours and days. Table 2 shows patient neurophysiological data from T1 and T2.
|
In 2 patients, MEPs were not elicitable from any of the stimulation sites on the AH at both T1 and T2 at maximal TCS intensity; this abnormality was fitting with the severe deficits substantiated by the low clinical scores. In another patient, MEPs were absent in T1; in T2 low-amplitude hand MEPs were elicitable from four scalp sites (ET, 90%). In this case, the hot spot showed an identical somatotopy on both AH and UH. This patient presented a consistent clinical amelioration in T2 versus T1 for both the Canadian Neurological Scale score (from 6.5 to 8) and the hand motor score (from 0 to 1). The ET of the UH (44.6±6.1%; range, 35% to 55%) was not statistically different from that of the control group. By contrast, the AH showed a significant (P<.001) increase in ET (68.8±19.9%) versus both the UH and the normal group.
First Recording Session (T1)
MEPs were absent from the AH in 3 patients, but they were always recordable after TCS of the UH. The number of scalp sites from which MEPs could be obtained was 4.5±1.6 in the UH and 2.4±1.5 in the AH (P<.05). The somatotopical organization of hand motor areas of both hemispheres is shown in Figs 2 and 3.
|
Four of 15 patients presented with the same hot-spot site on the two hemispheres. No consistent asymmetries with respect to normal subjects were found either on the sagittal or coronal planes except for 4 patients in whom anomalous hot-spot sites were found (2 on UH and 2 on AH, respectively; Fig 3).
|
MEP amplitudes from the hot spot showed a significant asymmetry (P<.001) between the UH (420±208 µV) and the AH (145±104 µV) despite the fact that higher intensities of TCS were used for the latter. Amplitude of MEPs from the hot spot recorded during contraction was 3381±1752 µV in the UH and 1096±1293 µV in the AH (P<.001). MEP latency was 21.7±2.0 milliseconds from the UH and 25.9±2.7 milliseconds from the AH (P<.001). Abnormally prolonged latencies were found in 7 of 12 patients. CCT was significantly prolonged (P<.001) from the AH (9.9±1.9 milliseconds) but in the normal range from the UH (7.1±1.4 milliseconds).
Second Recording Session (T2)
As observed in the control group during the retest recording session, the somatotopical mapping of the motor output area from the UH did not show significant variations. The average number of scalp sites from which MEPs were elicited was 4.4±1.7. In contrast, the AH was significantly more responsive during the T2 mapping session: the number of sites from which MEPs could be obtained was 3.2±1.8 (P<.05 with respect to T1). In 8 of 13 patients (excluding 2 patients with absent MEPs in T2), there were more excitable sites in T2 than in T1, with a consistent reorganization of the brain motor output during this poststroke epoch (2nd to 4th month). The somatotopy of ADM representation on the scalp did not show significant asymmetry on the sagittal and coronal planes when compared with the T1 session (Fig 2
).
In T2, anomalous hot-spot sites were more frequent than in T1 (4 on the AH and 5 on the UH). In particular, in 2 patients, changes in the shape of motor maps of the AH were "mirrored" on the UH also, maintaining a fairly symmetrical somatotopy (Fig 4).
MEP amplitudes were 432±247 and 256±226 µV for the UH and AH, respectively. Amplitudes of MEPs in the contracted condition were 3262±1292 and 1500±1568 µV (P<.001) in the UH and AH, respectively. MEP latencies from the UH and AH were 22.0±1.4 and 24.4±1.8 milliseconds (P<.001), respectively. CCTs were 7.2±0.9 milliseconds from the UH and 8.8±0.8 milliseconds from the AH (NS), with a net improvement with respect to T1. This shows that the output reorganization was utilizing fast-propagating, paucisynaptic connections, similar to the UH.
Cortical Versus Subcortical Lesions
Because of the relatively small size of the patient population, only one subgrouping in cortical and subcortical lesions was attempted.
First Recording Session (T1)
The number of responsive sites in the AH was 3.1±1.3 in the cortical and 1.5±1.7 in the subcortical lesions (P<.05). An anomalous hot-spot site was found in 3 cortical lesions and in 1 subcortical lesion. MEP latency in the AH was 23.7±1.2 and 27.8±3.1 milliseconds in cortical and subcortical lesions, respectively (P<.05).
Second Recording Session (T2)
The number of responsive sites in the AH was 3.8±2.1 in the cortical lesions and 3.3±2.5 in the subcortical lesions (NS). An anomalous hot-spot site in the AH was found in 6 patients, 4 of them being affected by a cortical lesion.
Clinical Score
Clinical scores are presented in Table 3. The hand motor score showed an amelioration between T1 and T2 in 11 of 15 patients. The functional evaluation (Barthel Index) showed an improvement in all the patients. The Canadian Neurological Scale score was increased in 13 of 15 patients. It is worth mentioning that those patients showing an enlargement of the hand area (more excitable sites in T2 than in T1) also showed a correlated improvement of the hand score (P<.05; r=.61). The level of lesion (cortical versus subcortical) did not influence the final clinical outcome.
|
Discussion |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
It is known that MEPs are heavily reduced in amplitude or entirely abolished after a hemispheric stroke.3 6 8 10 11 12 13 14 34 A few studies have correlated MEP characteristics in acute stroke with final clinical outcome.11 12 However, none of them addressed the question of whether recovery of motor function was based on reestablishment of previously damaged, but not destroyed, corticospinal connections or on "plastic" rearrangements of cortical somatotopy in which neuronal pools that are functionally silent or operating differently were substituting for the lost neurons. One way to approach this problem is to map the motor cortical output to partly paralyzed muscles and to the homologous ones on the undamaged side and observe the changes during recovery. Animal experiments have clearly shown that some plastic rearrangement of the central nervous system functions occurs in adulthood.35 Sanes et al36 reported a very rapid reorganization of motor cortical output in rats after facial nerve transection. Moreover, repeated mental simulation of movements is able to provoke an enlargement of motor maps that is similar to that which follows physical practice of the same movements.37 The wide distribution on the scalp of the excitable sites connected with ADM muscle might appear inconsistent with the commonly accepted anatomic maps. However, recent observation in awake patients undergoing cortical stimulation by subdural grid electrodes clearly showed that commonly accepted maps need to be reconsidered.38 39 Nii et al39 have shown in awake humans that hand motor responses to direct brain stimulation extend 4.7 cm anterior and 3.4 cm posterior to the central sulcus in an area 8.5 cm superior to the sylvian fissure. Therefore, focal stimulation on the scalp seems to provide a reliable picture of the cortical motor maps.
Brain functional imaging studies have described the recovery from hemiplegic stroke as associated with a marked reorganization of activation patterns of specific brain structures. Chollet et al40 and Weiller et al41 reported activation of hemispheric structures ipsilateral to the paretic side extending from premotor to motor cortex. Weder et al42 showed with PET techniques that during a programmed tactile exploration of shape in patients affected by subcortical ischemic infarction, there was a large activation of motor and sensory hand areas contralateral to the affected hand. However, it is hard to precisely discriminate the separate roles played by motor deficit, brain lesion, poor motor performance, and altered sensory perception in PET, SPECT, and even in functional MRI because of the length of the analysis time (from minutes to seconds) and the amount of motor activity needed to induce visible metabolic changes. Magnetic TCS permits the testing of the functional efficacy of corticospinal tracts governing a given target muscle and the mapping out of its cortical representation with a time discrimination of about 1 millisecond or less and a space discrimination on the scalp of 1 cm. To our knowledge, this is the first study in which maps of the motor output to an individual low-threshold, highly specialized hand muscle (ADM) were constructed and compared between the UH and AH of stroke patients versus a group of healthy volunteers and followed up over time. On the AH, ETs were significantly higher and MEP amplitudes smaller despite the stronger TCS that was used. The area of cortical output to the ADM muscle was significantly restricted compared with that of the UH.
It is noteworthy that when there was a subcortical lesion, the ET and scalp representation were remarkably more altered in the first recording session. This probably should be ascribed to the larger number of densely packed fibers destroyed by the lesion and possibly to a less efficient and slower "plastic" reorganization. Anomalous hot-spot sites were observed more frequently in the cortical than in the subcortical patient group and in T2 than in T1. We can argue that subcortical lesions are more sensitive to focal magnetic TCS than cortical ones in the 2 months after stroke and that the prognostic value of magnetic TCS is less reliable in subcortical than in cortical lesions in the relatively early phases of recovery from stroke. Finally, the recovery of cortical lesions with anomalous hot-spot sites might rely on the activation of brain areas outside the usual boundaries of the primary motor cortex. Therefore, these findings might represent a neurophysiological marker of plastic rearrangements of cortical output.
There was a significant enlargement of the hand motor cortical output area in T2, coupled with a clinical improvement documented by the amelioration of disability and neurological scores. MEP parameters and clinical scores were statistically correlated when the enlargement of hand motor cortical output area was considered (P<.05). MEP amplitude at rest and during voluntary contraction showed a consistent amelioration in the T2.
Experimental data suggest the existence of multiple motor cortical maps from primary as well as from supplementary motor and premotor cortices, with multiple descending corticospinal pathways with an orderly, topographically organized manner.43 Hence, the time course and degree of motor recovery in humans could largely depend on the amount of such multiple motor area lesioning, since different motor areas operate in a parallel rather than a hierarchical fashion. Moreover, they are able to functionally substitute for each other.44
MEP recording in early stages cannot always assess the amount of corticospinal tract fiber integrity because of enhanced ET and nerve impulse conduction block (partial or total) due to perilesional edema.14 The postlesional timing of our study is long enough to suggest that the observed modifications are due to corticospinal tract reorganization rather than recovery from perilesional edema and cortical hypoexcitability. Recovery of sensory deficits can also play a significant role, given the recently demonstrated strict relationship between topography of motor output and amount of sensory input.26
Our data suggest that a neurophysiological predictive pattern for poor recovery of arm-hand functionality is mainly related to the lack of MEPs at the maximum of magnetic TCS. Of the 3 patients with absent MEPs in T1, 1 showed MEP reappearance in T2 with a concomitant clinical recovery; in the other 2, recovery was poor when evaluated with a specific hand score.
A number of conclusions can be drawn on the basis of our observations concerning the central motor tract functionality as tested with magnetic TCS. (1) Between 2 and 4 months after a monohemispheric stroke, the motor output is still undergoing a remarkable reorganization for clinical recovery. (2) Such reorganization is mainly reflected by the enlargement of the excitable brain area and increased MEP amplitude. (3) Enlargement of the AH cortical motor output is usually developing inside the area normally devoted to control of the ADM muscle. However, in about 40% of cases, scalp sites never associated with ADM activation ("anomalous sites") respond to TCS. This probably reflects reorganization of corticospinal tracts via the involvement of neuronal pools usually not connected with ADM control and outside the "normal" excitable hand area of the brain. (4) The cortical motor output of the UH does not change significantly in control subjects or in T2 compared with T1. However, in 35% of cases, unusually active sites were found outside the scalp area normally connected with ADM. This was an isolated finding in 20% of cases; however, it was associated with similar changes on the AH in 35% of cases, possibly reflecting interhemispheric influences in addition to such restorative processes.
|
Selected Abbreviations and Acronyms |
|---|
|
|
Acknowledgments |
|---|
Funding for this study was provided by IRCCS S Lucia Institute, Rome, Italy.
Received July 9, 1996; revision received September 16, 1996; accepted September 19, 1996.
|
References |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
1. Merton PA, Morton HB. Stimulation of the cerebral cortex in intact human subjects. Nature. 1980;285:227. Letter.[Medline] [Order article via Infotrieve]
2. Rossini PM, Marciani MG, Caramia M, Roma V, Zarola F. Nervous propagation along central motor pathways in intact man: characteristics of motor responses to "bifocal" and "unifocal" spine and scalp stimulation. Electroenceph Clin Neurophysiol. 1985;61:272-286.[Medline] [Order article via Infotrieve]
3. Rossini PM, Caramia M, Zarola F. Central motor tract propagation in men: studies with non-invasive, unifocal scalp stimulation. Brain Res. 1987;415:211-225.[Medline] [Order article via Infotrieve]
4. Rossini PM, Barker T, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallet M, Katayama Y, Lucking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C. Noninvasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroenceph Clin Neurophysiol. 1994;91:79-92.[Medline] [Order article via Infotrieve]
5. Barker AT, Jalinous R, Freeston IL. Non-invasive stimulation of human motor cortex. Lancet. 1985;2:1106-1107.[Medline] [Order article via Infotrieve]
6.
Berardelli A, Inghilleri M, Formisano R, Accornero N, Manfredi M. Stimulation of motor tracts in motor neuron disease. J Neurol Neurosurg Psychiatry. 1987;50:732-737.
7.
Dominkus M, Grisold W, Jelinek V. Transcranial electric motor evoked potentials as a prognostic indicator for motor recovery in stroke patients. J Neurol Neurosurg Psychiatry. 1990;53:745-748.
8. MacDonnel RAL, Donnan GA, Bladin PF. A comparison of somatosensory evoked and motor evoked potentials in stroke. Ann Neurol. 1989;25:68-73.[Medline] [Order article via Infotrieve]
9. Hoemberg V, Stephan KM, Netz J. Transcranial stimulation of motor cortex in upper motor neurone syndrome: its relation to the motor deficit. Electroenceph Clin Neurophysiol. 1991;81:377-388.[Medline] [Order article via Infotrieve]
10. Caramia MD, Cicinelli P, Paradiso C, Mariorenzi R, Zarola F, Bernardi G, Rossini PM. `Excitability' changes of muscular responses to magnetic brain stimulation in patients with central motor disorders. Electroenceph Clin Neurophysiol. 1991;81:243-250.
11.
Heald A, Bates D, Cartlidge NEF, French JM, Miller S. Longitudinal study of central motor conduction time following stroke, I: natural history of central motor conduction. Brain. 1993;116:1355-1370.
12.
Heald A, Bates D, Cartlidge NEF, French JM, Miller S. Longitudinal study of central motor conduction time following stroke, II: central motor conduction measured within 72 h after stroke as a predictor of functional outcome at 12 months. Brain. 1993;116:1371-1385.
13. Catano A, Houa M, Caroyer JM, Ducarne H, Noel P. Magnetic transcranial stimulation in non-haemorrhagic stroke: interest of facilitation for early functional diagnosis. Electroenceph Clin Neurophysiol. 1995;97:349-354.[Medline] [Order article via Infotrieve]
14. Binkofski F, Seitz RJ, Arnold S, Classen J, Benecke R, Freund HJ. Thalamic metabolism and corticospinal tract integrity determine motor recovery in stroke. Ann Neurol. 1996;39:460-470.[Medline] [Order article via Infotrieve]
15. Arac N, Sagduyu A, Binai S, Ertekin C. Prognostic value of transcranial magnetic stimulation in acute stroke. Stroke. 1994;11:2183-2186.
16. Rossini PM, Caramia MD. Methodological and physiological considerations on the electric or magnetic transcranial stimulation. In: Rossini PM, Marsden CD, eds. Noninvasive Stimulation of Brain and Spinal Cord: Fundamentals and Clinical Applications. New York, NY: Alan R Liss; 1988:37-65.
17. Cohen LG, Hallett M, Lelli S. Noninvasive mapping of human motor cortex with transcranial magnetic stimulation. In: Chokroverty S, ed. Magnetic Stimulation in Clinical Neurophysiology. Stoneham, Mass: Butterworth Publishers; 1989:113-119.
18. Fuhr P, Cohen LG, Dang N, Findley TW, Haghighi S, Oro J, Hallet M. Physiological analysis of motor reorganization following lower limb amputation. Electroenceph Clin Neurophysiol. 1992;85:53-60.[Medline] [Order article via Infotrieve]
19. Mortifee P, Steward H, Schuler M, Eisen A. Reliability of transcranial magnetic stimulation for mapping the human motor cortex. Electroenceph Clin Neurophysiol. 1994;93:131-137.[Medline] [Order article via Infotrieve]
20. Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M. Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse and stimulus intensity. J Clin Neurophysiol. 1992;1:132-136.
21. Wilson SA, Thickbroom GW, Mastaglia FC. Transcranial magnetic stimulation mapping of the motor cortex in normal subjects. J Neurol Sci. 1993;118:134-144.[Medline] [Order article via Infotrieve]
22. Benecke R, Meyer BU, Freund HJ. Reorganization of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions demonstrated by magnetic brain stimulation. Exp Brain Res. 1991;83:419-426.[Medline] [Order article via Infotrieve]
23.
Topka H, Cohen LG, Cole RA, Hallett M. Reorganization of cortical spinal pathways following spinal injuries. Neurology. 1991;41:1276-1283.
24.
Cohen LG, Bendinelli S, Findlay TW, Hallett M. Motor reorganization after upper limb amputation in man. Brain. 1991;114:615-627.
25.
Brasil-Neto JP, Cohen LG, Pascual-Leon A, Jabir FK, Wall RT, Hallett M. Rapid reversible modulation of human motor outputs after transient deafferentation of the forearm: a study with transcranial magnetic stimulation. Neurology. 1994;42:1302-1306.
26. Rossini PM, Rossi S, Tecchio F, Pasqualetti P, Finozzi-Agro' A, Sabato A. Focal brain stimulation in healthy humans: preliminary report on upper limb motor maps changes following partial hand sensory deprivation. Neurosci Lett. 1996. In press.
27. Liepert J, Tegentholf M, Malin JP. Changes of cortical motor area size during immobilization. Electroenceph Clin Neurophysiol. 1996. In press.
28. Dromerick AW, Reding MJ. Functional outcome for patients with hemiparesis, hemihypesthesia, and hemianopsia. Stroke. 1995;11:2023-2026.
29. Mahoney FI, Barthel DW. Functional evaluation: the Barthel Index. Md State Med J. 1965;14:61-85.[Medline] [Order article via Infotrieve]
30.
Cote R, Hachinski VC, Shurvell BI, Norris JW, Wolfson C. The Canadian Neurological Scale: a preliminary study in acute stroke. Stroke. 1986;17:731-737.
31. Bobath B. Adult Hemiplegia: Evaluation and Treatment. 2nd ed. London, UK: William Heinemann Medical Books Ltd; 1970.
32. Cicinelli P, Traversa R, Bassi A, Scivoletto G, Rossini PM. Interhemispheric differences of hand muscle representation in human motor cortex. Muscle Nerve. 1996. In press.
33. Caramia MD, Pardal AM, Zarola F, Rossini PM. Neurophysiological evaluation of the central nervous impulse propagation in patients with sensorimotor disturbances. Brain Res. 1989;69:431-436.
34. Caramia MD, Bernardi G, Zarola F, Rossini PM. Neurophysiological evaluation of the central nervous impulse propagation in patients with sensorimotor disturbances. Electroenceph Clin Neurophysiol. 1988;70:16-25.[Medline] [Order article via Infotrieve]
35. Merzenich MM, Kaas JH, Wall JT, Sur M, Nelson RJ, Felleman DJ. Progression of change following median nerve section in the cortical representation of the hand areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience. 1983;10:639-665.[Medline] [Order article via Infotrieve]
36. Sanes JN, Suner S, Donoghue JP. Dynamic organization of primary motor cortex output to target muscles in adult rats: long-term patterns of reorganization following motor or mixed peripheral nerve lesions. Exp Brain Res. 1990;79:479-491.[Medline] [Order article via Infotrieve]
37.
Pascual-Leone A, Dang H, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol. 1995;74:1037-1045.
38. Uematsu S, Lesser RP, Gordon B. Localization of sensorimotor cortex: the influence of Sherrington and Cushing on the modern concept. Neurosurgery. 1992;30:904-913.[Medline] [Order article via Infotrieve]
39.
Nii Y, Uematsu S, Lesser RP, Gordon B. Does the central sulcus divide motor and sensory functions? Neurology. 1996;46:360-367.
40. Chollet F, Di Piero V, Wise RJS, Brooks DJ, Dolan RJ, Frackowiak SJ. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol. 1991;29:63-71.[Medline] [Order article via Infotrieve]
41. Weiller C, Ramsay S, Wise R, Friston K, Frackowiak SJ. Individual patterns of functional reorganization in the human cerebral cortex after capsular infarction. Ann Neurol. 1993;33:181-189.[Medline] [Order article via Infotrieve]
42.
Weder B, Knorr U, Herzog H, Nebeling B, Kleinschmidt A, Huang Y, Steinmetz H, Freund HJ, Seitz RJ. Tactile exploration of shape after subcortical ischaemic infarction studied with PET. Brain. 1994;117:593-605.
43. Strick PL. Anatomical organization of multiple motor areas in the frontal lobe: implications for recovery of function. Adv Neurol. 1988;47:293-312.[Medline] [Order article via Infotrieve]
44.
Fries W, Danek A, Scheidtmann K, Hamburger C. Motor recovery following capsular stroke: role of descending pathways from multiple motor areas. Brain. 1993;116:369-382.
This article has been cited by other articles:
 |
|
 |
|
  V. Di Lazzaro, P. Profice, F. Pilato, F. Capone, F. Ranieri, P. Pasqualetti, C. Colosimo, E. Pravata, A. Cianfoni, and M. Dileone Motor Cortex Plasticity Predicts Recovery in Acute Stroke Cereb Cortex, October 5, 2009; (2009) bhp216v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. R. Winship and T. H. Murphy Remapping the Somatosensory Cortex after Stroke: Insight from Imaging the Synapse to Network Neuroscientist, October 1, 2009; 15(5): 507 - 524. [Abstract] [PDF]
|
|
|
|
 |
|
 I B M Koesler, M Dafotakis, M Ameli, G R Fink, and D A Nowak Electrical somatosensory stimulation improves movement kinematics of the affected hand following stroke J. Neurol. Neurosurg. Psychiatry, June 1, 2009; 80(6): 614 - 619. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. Eisner-Janowicz, S. Barbay, E. Hoover, A. M. Stowe, S. B. Frost, E. J. Plautz, and R. J. Nudo Early and Late Changes in the Distal Forelimb Representation of the Supplementary Motor Area After Injury to Frontal Motor Areas in the Squirrel Monkey J Neurophysiol, September 1, 2008; 100(3): 1498 - 1512. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Manganotti, M. Acler, G. P. Zanette, N. Smania, and A. Fiaschi Motor Cortical Disinhibition During Early and Late Recovery After Stroke Neurorehabil Neural Repair, July 1, 2008; 22(4): 396 - 403. [Abstract] [PDF]
|
|
|
|
 |
|
 S. T. Carmichael Themes and Strategies for Studying the Biology of Stroke Recovery in the Poststroke Epoch Stroke, April 1, 2008; 39(4): 1380 - 1388. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Murata, N. Higo, T. Oishi, A. Yamashita, K. Matsuda, M. Hayashi, and S. Yamane Effects of Motor Training on the Recovery of Manual Dexterity After Primary Motor Cortex Lesion in Macaque Monkeys J Neurophysiol, February 1, 2008; 99(2): 773 - 786. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. N. McDonnell, S. L. Hillier, T. S. Miles, P. D. Thompson, and M. C. Ridding Influence of Combined Afferent Stimulation and Task-Specific Training Following Stroke: A Pilot Randomized Controlled Trial Neurorehabil Neural Repair, October 1, 2007; 21(5): 435 - 443. [Abstract] [PDF]
|
|
|
|
|
|
M Moller, J Frandsen, G Andersen, A Gjedde, P Vestergaard-Poulsen, and L Ostergaard Dynamic changes in corticospinal tracts after stroke detected by fibretracking J. Neurol. Neurosurg. Psychiatry, June 1, 2007; 78(6): 587 - 592. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. J Butler and S. L Wolf Putting the Brain on the Map: Use of Transcranial Magnetic Stimulation to Assess and Induce Cortical Plasticity of Upper-Extremity Movement Physical Therapy, June 1, 2007; 87(6): 719 - 736. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Desmurget, F. Bonnetblanc, and H. Duffau Contrasting acute and slow-growing lesions: a new door to brain plasticity Brain, April 1, 2007; 130(4): 898 - 914. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Mrachacz-Kersting, M. Fong, B. A. Murphy, and T. Sinkjaer Changes in Excitability of the Cortical Projections to the Human Tibialis Anterior After Paired Associative Stimulation J Neurophysiol, March 1, 2007; 97(3): 1951 - 1958. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Boake, E. A. Noser, T. Ro, S. Baraniuk, M. Gaber, R. Johnson, E. T. Salmeron, T. M. Tran, J. M. Lai, E. Taub, et al. Constraint-Induced Movement Therapy During Early Stroke Rehabilitation Neurorehabil Neural Repair, January 1, 2007; 21(1): 14 - 24. [Abstract] [PDF]
|
|
|
|
|
|
Y.-H. Kim, S. H. You, M.-H. Ko, J.-W. Park, K. H. Lee, S. H. Jang, W.-K. Yoo, and M. Hallett Repetitive Transcranial Magnetic Stimulation-Induced Corticomotor Excitability and Associated Motor Skill Acquisition in Chronic Stroke Stroke, June 1, 2006; 37(6): 1471 - 1476. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Hummel, P. Celnik, P. Giraux, A. Floel, W.-H. Wu, C. Gerloff, and L. G. Cohen Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke Brain, March 1, 2005; 128(3): 490 - 499. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Koski, T. J. Mernar, and B. H. Dobkin Immediate and Long-Term Changes in Corticomotor Output in Response to Rehabilitation: Correlation with Functional Improvements in Chronic Stroke Neurorehabil Neural Repair, December 1, 2004; 18(4): 230 - 249. [Abstract] [PDF]
|
|
|
|
 |
|
 L. H.A. Strens, P. Asselman, A. Pogosyan, C. Loukas, A. J. Thompson, and P. Brown Corticocortical coupling in chronic stroke: Its relevance to recovery Neurology, August 10, 2004; 63(3): 475 - 484. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. M. Butefisch Plasticity in the Human Cerebral Cortex: Lessons from the Normal Brain and from Stroke Neuroscientist, April 1, 2004; 10(2): 163 - 173. [Abstract] [PDF]
|
|
|
|
|
|
M. Kobayashi, S. Hutchinson, H. Theoret, G. Schlaug, and A. Pascual-Leone Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements Neurology, January 13, 2004; 62(1): 91 - 98. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. H Crosbie, S. M McDonough, D. H Gilmore, and M I. Wiggam The adjunctive role of mental practice in the rehabilitation of the upper limb after hemiplegic stroke: a pilot studya Clinical Rehabilitation, January 1, 2004; 18(1): 60 - 68. [Abstract] [PDF]
|
|
|
|
|
|
N. S. Ward, M. M. Brown, A. J. Thompson, and R. S. J. Frackowiak Neural correlates of motor recovery after stroke: a longitudinal fMRI study Brain, November 1, 2003; 126(11): 2476 - 2496. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. B. Frost, S. Barbay, K. M. Friel, E. J. Plautz, and R. J. Nudo Reorganization of Remote Cortical Regions After Ischemic Brain Injury: A Potential Substrate for Stroke Recovery J Neurophysiol, June 1, 2003; 89(6): 3205 - 3214. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. F. Wittenberg, R. Chen, K. Ishii, K. O. Bushara, E. Taub, L. H. Gerber, M. Hallett, and L. G. Cohen Constraint-Induced Therapy in Stroke: Magnetic-Stimulation Motor Maps and Cerebral Activation Neurorehabil Neural Repair, March 1, 2003; 17(1): 48 - 57. [Abstract] [PDF]
|
|
|
|
|
|
J. L. Tillerson and G. W. Miller Book Review: Forced Limb-Use and Recovery following Brain Injury Neuroscientist, December 1, 2002; 8(6): 574 - 585. [Abstract] [PDF]
|
|
|
|
|
|
H. Johansen-Berg, H. Dawes, C. Guy, S. M. Smith, D. T. Wade, and P. M. Matthews Correlation between motor improvements and altered fMRI activity after rehabilitative therapy Brain, December 1, 2002; 125(12): 2731 - 2742. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. P. Bastings, J. P. Greenberg, and D. C. Good Hand Motor Recovery after Stroke: A Transcranial Magnetic Stimulation Mapping Study of Motor Output Areas and Their Relation to Functional Status Neurorehabil Neural Repair, September 1, 2002; 16(3): 275 - 282. [Abstract] [PDF]
|
|
|
|
|
|
T. Shimizu, A. Hosaki, T. Hino, M. Sato, T. Komori, S. Hirai, and P. M. Rossini Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke Brain, August 1, 2002; 125(8): 1896 - 1907. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S J BONIFACE Plasticity after acute ischaemic stroke studied by transcranial magnetic stimulation J. Neurol. Neurosurg. Psychiatry, December 1, 2001; 71(6): 713 - 715. [Full Text] [PDF]
|
|
|
|
 |
|
 S C Cramer, E Fray, A Tievsky, R A Parker, P N Riskind, M C Stein, V Wedeen, and B R Rosen Changes in motor cortex activation after recovery from spinal cord inflammation Multiple Sclerosis, December 1, 2001; 7(6): 364 - 370. [Abstract] [PDF]
|
|
|
|
 |
|
 B. Pleger, H. R. Dinse, P. Ragert, P. Schwenkreis, J. P. Malin, and M. Tegenthoff Shifts in cortical representations predict human discrimination improvement PNAS, September 26, 2001; (2001) 191176298. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. M. Filippi, M. Oliveri, P. Pasqualetti, P. Cicinelli, R. Traversa, F. Vernieri, M. G. Palmieri, and P. M. Rossini Effects of motor imagery on motor cortical output topography in Parkinson's disease Neurology, July 10, 2001; 57(1): 55 - 61. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Kern, R. Birn, S. Jaradeh, A. Jesmanowicz, R. Cox, J. Hyde, and R. Shaker Swallow-related cerebral cortical activity maps are not specific to deglutition Am J Physiol Gastrointest Liver Physiol, April 1, 2001; 280(4): G531 - G538. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Liepert, H. Bauder, W. H. R. Miltner, E. Taub, and C. Weiller Treatment-Induced Cortical Reorganization After Stroke in Humans Stroke, June 1, 2000; 31(6): 1210 - 1216. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. C. Cramer, C. I. Moore, S. P. Finklestein, and B. R. Rosen A Pilot Study of Somatotopic Mapping After Cortical Infarct Stroke, March 1, 2000; 31(3): 668 - 671. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Oliveri, P. M. Rossini, P. Pasqualetti, R. Traversa, P. Cicinelli, M. G. Palmieri, F. Tomaiuolo, and C. Caltagirone Interhemispheric asymmetries in the perception of unimanual and bimanual cutaneous stimuli: A study using transcranial magnetic stimulation Brain, September 1, 1999; 122(9): 1721 - 1729. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. V. Escudero, J. Sancho, D. Bautista, M. Escudero, and J. Lopez-Trigo Prognostic Value of Motor Evoked Potential Obtained by Transcranial Magnetic Brain Stimulation in Motor Function Recovery in Patients With Acute Ischemic Stroke Stroke, September 1, 1998; 29(9): 1854 - 1859. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. C. Cramer, G. Nelles, R. R. Benson, J. D. Kaplan, R. A. Parker, K. K. Kwong, D. N. Kennedy, S. P. Finklestein, and B. R. Rosen A Functional MRI Study of Subjects Recovered From Hemiparetic Stroke Stroke, December 1, 1997; 28(12): 2518 - 2527. [Abstract] [Full Text]
|
|
|
|
|
|
B. Pleger, H. R. Dinse, P. Ragert, P. Schwenkreis, J. P. Malin, and M. Tegenthoff Shifts in cortical representations predict human discrimination improvement PNAS, October 9, 2001; 98(21): 12255 - 12260. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||