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Motor evoked potentials of the human diaphragm elicited through magnetic transcranial brain stimulation
3OURNAL OF THE
NEUROLOGICAL SCIENCES ELSEVIER
Journal of the Neurological Sciences 124 (1994) 204-207
Motor evoked potentials of the human diaphragm elicited through magnetic transcranial brain stimulation Mark A. Lissens * Department of Physical Medicine and Rehabilitation, Unit,ersity Hospital, Gent, Belgium, and Dit:ision of Restoratit,e Neurology and Human Neurobiology, Baylor College of Medicine, Houston, TX, USA (Received 2 November 1993; revised 28 January 1994; accepted 2 February 1994)
Abstract
Magnetic transcranial brain stimulation has been used for several years now to study the function and integrity o f the corticospinal tracts. In this study magnetic transcranial motor cortex stimulation of the diaphragm was carried out in order to describe the characteristics of the recorded motor evoked potentials (MEPs) of this muscle in humans. The motor cortex was stimulated transcranially in 10 healthy subjects, followed by stimulation of the cervical roots so that central motor conduction time (CMCT) could be calculated. Diaphragm MEPs were recorded at deep inspiration. Normal values were found to be t6.21 + 0.33 msec for the MEP latency time, 3.52 _+ 2.40 mV for the MEP amplitude, and 8.39 _+0.41 msec. for the CMCT. This study confirms the direct projection from the motor cortex to the human diaphragm and the ability of cortical magnetic stimuli to evoke more descending volleys along the corticospinal pathways. This technique can offer useful additional information about the function and integrity of central motor conduction properties of respiratory muscles in humans with various neurological and respiratory disorders.
Key words: Diaphragm; Magnetic transcranial stimulation; Motor cortex; Motor evoked potentials (MEPs); Phrenic nerve; Respiratory muscles
1. I n t r o d u c t i o n
Since magnetic transcranial brain stimulation was introduced in 1985 (Barker et al. 1985) to study the integrity of the corticospinal tracts, quite a few clinical applications (Lissens 1992) became available. Especially because it could be performed without any discomfort to the patient, it was applied instead of the more painful electrical transcranial stimulation (Merton and Morton 1980) in various neurological disorders as well as for neuromonitoring of comatose patients (Firsching et al. 1990; Rohde et al. 1991), during surgery (Jellinek et al. 1992; Shields et al. 1990), and in rehabilitation medicine (Dimitrijevic et al. 1990; H u m -
* Correspondence to: Gent University Hospital, Department of Physical Medicine and Rehabilitation, Poli 5, De Pintelaan 185, B-9000 Ghent, Belgium. Tel.: ( + 32-9) 240 2234; Fax: ( + 32-9) 240 4975. 0022-510X/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved
SSDI 0 0 2 2 - 5 1 0 X ( 9 4 ) 0 0 0 4 7 - R
melsheim et al. 1992). In most studies motor evoked potentials (MEPs) were recorded only from muscles of u p p e r and lower extremities. In 1986 Gandevia et al. stimulated the diaphragm by electrical transcranial stimulation at the vertex (in only 3 subjects) using a rather invasive recording technique through a gastro-oesophageal catheter. So far, no systematic M E P study with magnetic transcranial stimulation (TCS) of respiratory muscles has been published. Guz et al. (1991) determined the site to be stimulated on the scalp, but they did not record MEPs n o r did they describe M E P characteristics such as latency time, amplitude, and central motor conduction time (CMCT). On the other hand magnetic bilateral peripheral phrenic nerve stimulation was reported by Similowski et al. (1989). The aim of this study was to obtain information about the central motor conduction properties of the respiratory muscles, especially the diaphragm, using a
.~I..1
li~scvl~/l~rt
~l~{ftte
124 ( I 0 ~ ) 4 ) _~0 4
M'~rol¢~gical.~licplce~
_()> " -
_0. • "
D i a p h r a g m - MEP's at increasing stimulus s t r e n g t h ..................................................
non-inwtsive and easily applicable technique, which would be very useful in various neurological and respiratory disorders affecting thcsc muscles.
487
!
2. Material and methods Fcn health\ voluntccrs, 5 males and 5 females, ranging in age from 20-30 years (mean 25.3), without any history of neurological or respiratow disease, were studied. Transcranial stimulation was delivered by a circular magnctic coil (outer diameter 12.5 cm) supplied with a Magstim 20(1 slimulator (Magstim Company, Whitland, UK) with a maximum (100<~) output of 2.5 tesla.
j
~
F 2 mV L - I0 msec
A,
C3
80z
17',, Right
Left
Fig. 2. Diaphragm motor evoked potentiab, (Mf{Ps) al incruasing stlnlulus slrcl]glh ot the magnelic stinluhlh~r. C4
Left
Fig. 1. Three Sl.lpelimposcd right and h.'ft diaphragm MEPs at 100c; stimulalion output ol the magnetic stimulalor, after left (C3) and right (('4) hemisphcre stimulation. Ualibralions are 5 msec/div, and 2 mV .
Motor evoked potentials (MEPs) were recorded with cup electrodes (0.5 cm), with the active electrode at the xiphoid process, the reference electrode tm the h)wer border of the rib cage at the midclavicular line, and thc ground clectrode at the manubrium stcrni. This recording method is to bc prcfcrrcd as has bcen shown in othcr studies of phrenic nerve conduction (Bolton 1993a,b: Wiesner ct al. 1~,'88). Magnetic transcranial stinlulation (TCS) was performed at 2 cm anterior to C 3 / C 4 (according to the 1(t-2() international system for placement of EEG clectrodcs) for lhc right and Icf( hemidiaphragm as shown by (;uz c t a l . (Igql). Subsequently, the cervical roots wcrc stinmlatcd at (74 level so that the central motor conduction time could bc calculated. All stimuli wcrc repeated 3 timcs (see Fig, 1). Thc MEPs were recordcd on an clcctromyograph ( M c d e l c c / T e c a Saffire 2M) with a filter setting of 3 Hz to 2 kHz. All subjects werc seated in a slightly supinc position in a comfortable chair and stimulation was performed
206
M.A. Lissens /Journal q["the Neurological Sciences 124 (1994) 204-207
on maximal deep inspiration, because with the above described recording technique amplitude is greatest during inspiration (Bolton 1993a; Day et al. 1987).
3. Results The mean latency time after magnetic TCS was found to be 16.21 + 0.33 msec, and the mean CMCT 8.39 + 0.41 msec. No significant differences were seen between the left and right side, nor between males (16.03 msec) and females (16.t4 msec). The mean peak-to-peak amplitude of the diaphragmatic MEPs was to be 3.52 + 2.40 mV. The stimulation threshold varied between 40 and 60% of maximal output. In most subjects maximum amplitude of the M E P was obtained at 8 0 - 9 0 % of maximum output. The amplitude increased and the latency time shortened at increasing stimulus output (see Fig. 2) the same way as has been shown in upper and lower limb muscles.
4. Discussion Magnetic transcraniat stimulation of the brain confirmed the direct projection from the motor cortex to the human diaphragm, similarly as was demonstrated for the corticospinal pathways to the limb muscles. It can be concluded that magnetic transcranial brain stimulation activates phrenic motor nuclei via rapidly conducting mono- or oligosynaptic pathways from the motor cortex to the human inspiratory motoneurons. As compared to the study by Gandevia et al. the M E P latency time and C M C T of our study were some 3 - 4 msec longer (16.2 vs. 12.3). This was to be expected, as latency times after magnetic TCS have been shown to be a few milliseconds longer than after electrical TCS (Barker et al. 1987), due to the different localisation of initially stimulated structures through cortico-cortical connections (Day et al, 1987). On the other hand, inhibitory and facilitating mechanisms have an important influence in magnetic TCS. Moreover, we used a different recording technique (surface electrodes at xiphoid process versus a gastro-esophageal probe in the study by Gandevia et al.). The standard deviation (SD) was very small, as well for the M E P latency times of the diaphragm as for the CMCT, whereas the SD of the amplitude showed a much larger variability. This makes the latency time a n d C M C T a very reliable parameter in the diagnosis and follow-up of neurological and respiratory disorders affecting the central motor conduction properties of the diaphragm. This small variability of latency times can be explained by the possible absence of any relay in ponto-medullary respiratory centers or by a lower number of central connections (Lipski et al. 1986), and
by the course of the phrenic nerve, which is the second largest nerve in the human body. Spinal stimulation in our study did not excite the motor axons distal to their exit from the spinal canal, because the latency to stimulation of the phrenic nerve ~Newsom-Davis 1967: Markand et al. 1984: Gandevia et al. 1987: Wiesner ct al. 1988; Swenson et al. 19921 was a few msec tcss than to spinal stimulation. The amplitude on the other hand depends on several local factors, such as skin thickness, underlying layers of fat and connective tissue, and interindividual differences of thorax and rib cage configuration and volume, which might at least partially explain the larger variability. However. the MEP amplitudes generally exceeded those produced by supramaximal stimulation of the phrenic nerves. This finding cannot only be explained by the possible activation of other synergistic inspiratory muscles, but also reflects the ability of the cortical magnetic stimuli to evoke more than one descending volley along the corticospinal pathways (Day et al. 1987). In conclusion, magnetic TCS is a painless and easily applicable technique to investigate the central motor conduction properties of the diaphragm, both in normal humans and in patients with various neurological and respiratory disorders. MEP latency time and CMCT in particular can be used as a rigid parameter in the diagnosis and follow-up of these diseases.
References Barker, A.T., Jalinous, R. and Freeston. l.k (19851 Non-invasive magnetic stimulation of the human motor cortex. Lancet. i: 1106-1107. Barker, A.T., Freeston, I.L.. Jalinous, R. and Jarrat, J.A (19871 Magnetic stimulation of the human brain and peripheral nervous system: an introduction and the results of an initial clinical evaluation. Neurosurgery, 20: 100-109. Bolton, C.F. (1993a) Clinical neurophysiology of the respiratory system. Muscle Nerve. 16: 809-818. Bolton, C.F. (1993b) EMG in the critical care unit. In: Brown. W.1. and Bolton, C.F. (Eds.), Clinical Electromyography, 2nd edn.. Butterworths, Boston. MA, pp. 759-773. Day, B.L., Thompson, P.D.. Dick. J.P.. Nakashima. K. and Marsden. C.D. (1987) Different sites of action of electrical and magnetic stimulation of the human brain. Neurosci. Lett.. 75/t: 101-106. Dimitrijevic, M.R., Lissens. M.A. and McKay, W,B. (19901 Characteristics and extent of motor activity recovery after spinal cord injury. In: Seil, F.J. (Ed.). Advances in Neural Regeneration Research, Wiley-Liss. New York. NY. pp. 391-405. Firsching, R. and Frowein. R.A. (19901 Multimodalityevoked potentials in early prognosis in comatose patients. Neurosurg. Rev.. 13: 141-146. Gandevia, S.C. and Rothwell. J.C. ~1987) Activation of the human diaphragm from the motor cortex. J. Physiol.. 384: 109-118. Guz, A. (1991) Studies on the human cortex and breathing: the utility of magnetic transcranial stimulation of the brain. Proceedings of Physiological Society, Charing Cross and Westminster Meeting, London, 10-11 January 1991, pp. lOP-lIP.
M..4. Lis'sens / J o u r n a [ q[" Hze M'uroD~ical Scicn( es' 124 (1074) 204 - 2(17
Ilurnnlclshcinl, 11.. Miinch. B., I:lutefisch, C.. ttoppc. S. and Neumann, S. (IqO2l Transcranial magnetic stimulation in rehabiliialion and physiotherapy evaluation in hemiparetic stroke patients. In: Lisscns. M . \ . (Ed.), Clinical Applications of Magnetic Transcranial Sfinml;ition, Pccicls Press, Leuven, Belgium, pp. 29113(1{I. h_'llinck, l).. ,lo~kcs, 1). ailcJ ,'qymon. k. (19gll) Noninvasivc iniraq~pcralivc illoi/ilOlillg of i11olor ew~kcd polenticils under pl~pofl)l allclcMhcxia; trice'is of Sl)imiJ surgery tin the amplitude tllld lalellC}, of ill~,)lor cv()kcd potcnlials. Nt.,tlro-surgery, 2t,l: 551-557. I_ipski, ,I., I+>¢kt;is. ,,\. and Porter, R. (1986) Short latency inpul, s It) phrcnic illt)ltHluill(llleS ii'11ill the scnsl)iin]otor cortex [i1 the c{it. I(xp. P,r;iiil I)xc.~. I~l: 2Sll 2qll. Mark~intl. ().IN.. Kincaid. J.('., P+,)Ul-lllalld. R.A., Moorthy, S.S., King. t<1.1)., M(ihanlc'ct, "l'. culd [+lrowi1, J.'~'. (1984) Electrophysiologic c\ahlclliOll ~)1 dial)hragm by tlan~.ctlt~ln~+'OtlS pt~renic nei~c stimu lillion. Nctlil>lo~_~, 34:6114 f~14. Mcrlon, I'.,.\. clnd ]MortolL l i B . (lt,iSl)) ,Stimulation of the cci-cbrill c'ltitcx in the intact htlnl{lll subject, N{ilui'e, 295: 277. NcwsOnl-l):lxis, .I.
2()7
Rohdc, V. and Zcntner. J. (1991) PrognoMic ;alu¢ ol motor evoked potentials in traumatic and nontraumatic ci)m;i. |it: Advances in Neurosurgery, vol. 19. Springcr-Verlag. Berlin. New York, pp. 194 20ft. Shielcls, C.B., Palohcimo, M.P.J., Backman. M.tt.. tLdmonds, I I.L. and Johnson, J.R. (1991)) |ntra~pctatixc use ol tianscranial magnetic m~tor evoked potentials. In: ('hokro;crt3, S. (t(d.), Magnctic Stimulation in Clinical Neurophysi~log~,. Butlcc, v(~rths. Boston London, pp. 173--184. Sinlihw~ski, T., Fleury, B., Laumois, S., ('alhala, t I.P., Bouchc, P. and Derennc. J.P. (Icj89) Cervical nlagnetic stinlulatinn: a new pain Icss method for bilateral phrenic neiac stimulatkm in ¢onsci~ms humans. ,I. AV,pl. Physiol., ~7(41:1311 131s. Swcnson. M R . and Rubcnstein. R.S. (l~,lc)21 Phrcnic nur\c comtuc lion studies. Muscle Ner¢c, 15:5~17 6113. Wiesncr. NIL. Sienlpien. L . M arid Maclcan. I.('. (19SN) Phrcnic ]lt.~i~.e conduction: The effect tH diaphragnmtic Disiti~m on the compound intlscl¢ aciioll polclllial. ]>il)cccdings o l the /\lllltlill Mucling o l the ,,\mcrican z\c~lclc'i/1~, iq Ph\sical Medicine :iilcl Rchahililalion, SCallle, X,VA, p 12t).
NEUROLOGICAL SCIENCES ELSEVIER
Journal of the Neurological Sciences 124 (1994) 204-207
Motor evoked potentials of the human diaphragm elicited through magnetic transcranial brain stimulation Mark A. Lissens * Department of Physical Medicine and Rehabilitation, Unit,ersity Hospital, Gent, Belgium, and Dit:ision of Restoratit,e Neurology and Human Neurobiology, Baylor College of Medicine, Houston, TX, USA (Received 2 November 1993; revised 28 January 1994; accepted 2 February 1994)
Abstract
Magnetic transcranial brain stimulation has been used for several years now to study the function and integrity o f the corticospinal tracts. In this study magnetic transcranial motor cortex stimulation of the diaphragm was carried out in order to describe the characteristics of the recorded motor evoked potentials (MEPs) of this muscle in humans. The motor cortex was stimulated transcranially in 10 healthy subjects, followed by stimulation of the cervical roots so that central motor conduction time (CMCT) could be calculated. Diaphragm MEPs were recorded at deep inspiration. Normal values were found to be t6.21 + 0.33 msec for the MEP latency time, 3.52 _+ 2.40 mV for the MEP amplitude, and 8.39 _+0.41 msec. for the CMCT. This study confirms the direct projection from the motor cortex to the human diaphragm and the ability of cortical magnetic stimuli to evoke more descending volleys along the corticospinal pathways. This technique can offer useful additional information about the function and integrity of central motor conduction properties of respiratory muscles in humans with various neurological and respiratory disorders.
Key words: Diaphragm; Magnetic transcranial stimulation; Motor cortex; Motor evoked potentials (MEPs); Phrenic nerve; Respiratory muscles
1. I n t r o d u c t i o n
Since magnetic transcranial brain stimulation was introduced in 1985 (Barker et al. 1985) to study the integrity of the corticospinal tracts, quite a few clinical applications (Lissens 1992) became available. Especially because it could be performed without any discomfort to the patient, it was applied instead of the more painful electrical transcranial stimulation (Merton and Morton 1980) in various neurological disorders as well as for neuromonitoring of comatose patients (Firsching et al. 1990; Rohde et al. 1991), during surgery (Jellinek et al. 1992; Shields et al. 1990), and in rehabilitation medicine (Dimitrijevic et al. 1990; H u m -
* Correspondence to: Gent University Hospital, Department of Physical Medicine and Rehabilitation, Poli 5, De Pintelaan 185, B-9000 Ghent, Belgium. Tel.: ( + 32-9) 240 2234; Fax: ( + 32-9) 240 4975. 0022-510X/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved
SSDI 0 0 2 2 - 5 1 0 X ( 9 4 ) 0 0 0 4 7 - R
melsheim et al. 1992). In most studies motor evoked potentials (MEPs) were recorded only from muscles of u p p e r and lower extremities. In 1986 Gandevia et al. stimulated the diaphragm by electrical transcranial stimulation at the vertex (in only 3 subjects) using a rather invasive recording technique through a gastro-oesophageal catheter. So far, no systematic M E P study with magnetic transcranial stimulation (TCS) of respiratory muscles has been published. Guz et al. (1991) determined the site to be stimulated on the scalp, but they did not record MEPs n o r did they describe M E P characteristics such as latency time, amplitude, and central motor conduction time (CMCT). On the other hand magnetic bilateral peripheral phrenic nerve stimulation was reported by Similowski et al. (1989). The aim of this study was to obtain information about the central motor conduction properties of the respiratory muscles, especially the diaphragm, using a
.~I..1
li~scvl~/l~rt
~l~{ftte
124 ( I 0 ~ ) 4 ) _~0 4
M'~rol¢~gical.~licplce~
_()> " -
_0. • "
D i a p h r a g m - MEP's at increasing stimulus s t r e n g t h ..................................................
non-inwtsive and easily applicable technique, which would be very useful in various neurological and respiratory disorders affecting thcsc muscles.
487
!
2. Material and methods Fcn health\ voluntccrs, 5 males and 5 females, ranging in age from 20-30 years (mean 25.3), without any history of neurological or respiratow disease, were studied. Transcranial stimulation was delivered by a circular magnctic coil (outer diameter 12.5 cm) supplied with a Magstim 20(1 slimulator (Magstim Company, Whitland, UK) with a maximum (100<~) output of 2.5 tesla.
j
~
F 2 mV L - I0 msec
A,
C3
80z
17',, Right
Left
Fig. 2. Diaphragm motor evoked potentiab, (Mf{Ps) al incruasing stlnlulus slrcl]glh ot the magnelic stinluhlh~r. C4
Left
Fig. 1. Three Sl.lpelimposcd right and h.'ft diaphragm MEPs at 100c; stimulalion output ol the magnetic stimulalor, after left (C3) and right (('4) hemisphcre stimulation. Ualibralions are 5 msec/div, and 2 mV .
Motor evoked potentials (MEPs) were recorded with cup electrodes (0.5 cm), with the active electrode at the xiphoid process, the reference electrode tm the h)wer border of the rib cage at the midclavicular line, and thc ground clectrode at the manubrium stcrni. This recording method is to bc prcfcrrcd as has bcen shown in othcr studies of phrenic nerve conduction (Bolton 1993a,b: Wiesner ct al. 1~,'88). Magnetic transcranial stinlulation (TCS) was performed at 2 cm anterior to C 3 / C 4 (according to the 1(t-2() international system for placement of EEG clectrodcs) for lhc right and Icf( hemidiaphragm as shown by (;uz c t a l . (Igql). Subsequently, the cervical roots wcrc stinmlatcd at (74 level so that the central motor conduction time could bc calculated. All stimuli wcrc repeated 3 timcs (see Fig, 1). Thc MEPs were recordcd on an clcctromyograph ( M c d e l c c / T e c a Saffire 2M) with a filter setting of 3 Hz to 2 kHz. All subjects werc seated in a slightly supinc position in a comfortable chair and stimulation was performed
206
M.A. Lissens /Journal q["the Neurological Sciences 124 (1994) 204-207
on maximal deep inspiration, because with the above described recording technique amplitude is greatest during inspiration (Bolton 1993a; Day et al. 1987).
3. Results The mean latency time after magnetic TCS was found to be 16.21 + 0.33 msec, and the mean CMCT 8.39 + 0.41 msec. No significant differences were seen between the left and right side, nor between males (16.03 msec) and females (16.t4 msec). The mean peak-to-peak amplitude of the diaphragmatic MEPs was to be 3.52 + 2.40 mV. The stimulation threshold varied between 40 and 60% of maximal output. In most subjects maximum amplitude of the M E P was obtained at 8 0 - 9 0 % of maximum output. The amplitude increased and the latency time shortened at increasing stimulus output (see Fig. 2) the same way as has been shown in upper and lower limb muscles.
4. Discussion Magnetic transcraniat stimulation of the brain confirmed the direct projection from the motor cortex to the human diaphragm, similarly as was demonstrated for the corticospinal pathways to the limb muscles. It can be concluded that magnetic transcranial brain stimulation activates phrenic motor nuclei via rapidly conducting mono- or oligosynaptic pathways from the motor cortex to the human inspiratory motoneurons. As compared to the study by Gandevia et al. the M E P latency time and C M C T of our study were some 3 - 4 msec longer (16.2 vs. 12.3). This was to be expected, as latency times after magnetic TCS have been shown to be a few milliseconds longer than after electrical TCS (Barker et al. 1987), due to the different localisation of initially stimulated structures through cortico-cortical connections (Day et al, 1987). On the other hand, inhibitory and facilitating mechanisms have an important influence in magnetic TCS. Moreover, we used a different recording technique (surface electrodes at xiphoid process versus a gastro-esophageal probe in the study by Gandevia et al.). The standard deviation (SD) was very small, as well for the M E P latency times of the diaphragm as for the CMCT, whereas the SD of the amplitude showed a much larger variability. This makes the latency time a n d C M C T a very reliable parameter in the diagnosis and follow-up of neurological and respiratory disorders affecting the central motor conduction properties of the diaphragm. This small variability of latency times can be explained by the possible absence of any relay in ponto-medullary respiratory centers or by a lower number of central connections (Lipski et al. 1986), and
by the course of the phrenic nerve, which is the second largest nerve in the human body. Spinal stimulation in our study did not excite the motor axons distal to their exit from the spinal canal, because the latency to stimulation of the phrenic nerve ~Newsom-Davis 1967: Markand et al. 1984: Gandevia et al. 1987: Wiesner ct al. 1988; Swenson et al. 19921 was a few msec tcss than to spinal stimulation. The amplitude on the other hand depends on several local factors, such as skin thickness, underlying layers of fat and connective tissue, and interindividual differences of thorax and rib cage configuration and volume, which might at least partially explain the larger variability. However. the MEP amplitudes generally exceeded those produced by supramaximal stimulation of the phrenic nerves. This finding cannot only be explained by the possible activation of other synergistic inspiratory muscles, but also reflects the ability of the cortical magnetic stimuli to evoke more than one descending volley along the corticospinal pathways (Day et al. 1987). In conclusion, magnetic TCS is a painless and easily applicable technique to investigate the central motor conduction properties of the diaphragm, both in normal humans and in patients with various neurological and respiratory disorders. MEP latency time and CMCT in particular can be used as a rigid parameter in the diagnosis and follow-up of these diseases.
References Barker, A.T., Jalinous, R. and Freeston. l.k (19851 Non-invasive magnetic stimulation of the human motor cortex. Lancet. i: 1106-1107. Barker, A.T., Freeston, I.L.. Jalinous, R. and Jarrat, J.A (19871 Magnetic stimulation of the human brain and peripheral nervous system: an introduction and the results of an initial clinical evaluation. Neurosurgery, 20: 100-109. Bolton, C.F. (1993a) Clinical neurophysiology of the respiratory system. Muscle Nerve. 16: 809-818. Bolton, C.F. (1993b) EMG in the critical care unit. In: Brown. W.1. and Bolton, C.F. (Eds.), Clinical Electromyography, 2nd edn.. Butterworths, Boston. MA, pp. 759-773. Day, B.L., Thompson, P.D.. Dick. J.P.. Nakashima. K. and Marsden. C.D. (1987) Different sites of action of electrical and magnetic stimulation of the human brain. Neurosci. Lett.. 75/t: 101-106. Dimitrijevic, M.R., Lissens. M.A. and McKay, W,B. (19901 Characteristics and extent of motor activity recovery after spinal cord injury. In: Seil, F.J. (Ed.). Advances in Neural Regeneration Research, Wiley-Liss. New York. NY. pp. 391-405. Firsching, R. and Frowein. R.A. (19901 Multimodalityevoked potentials in early prognosis in comatose patients. Neurosurg. Rev.. 13: 141-146. Gandevia, S.C. and Rothwell. J.C. ~1987) Activation of the human diaphragm from the motor cortex. J. Physiol.. 384: 109-118. Guz, A. (1991) Studies on the human cortex and breathing: the utility of magnetic transcranial stimulation of the brain. Proceedings of Physiological Society, Charing Cross and Westminster Meeting, London, 10-11 January 1991, pp. lOP-lIP.
M..4. Lis'sens / J o u r n a [ q[" Hze M'uroD~ical Scicn( es' 124 (1074) 204 - 2(17
Ilurnnlclshcinl, 11.. Miinch. B., I:lutefisch, C.. ttoppc. S. and Neumann, S. (IqO2l Transcranial magnetic stimulation in rehabiliialion and physiotherapy evaluation in hemiparetic stroke patients. In: Lisscns. M . \ . (Ed.), Clinical Applications of Magnetic Transcranial Sfinml;ition, Pccicls Press, Leuven, Belgium, pp. 29113(1{I. h_'llinck, l).. ,lo~kcs, 1). ailcJ ,'qymon. k. (19gll) Noninvasivc iniraq~pcralivc illoi/ilOlillg of i11olor ew~kcd polenticils under pl~pofl)l allclcMhcxia; trice'is of Sl)imiJ surgery tin the amplitude tllld lalellC}, of ill~,)lor cv()kcd potcnlials. Nt.,tlro-surgery, 2t,l: 551-557. I_ipski, ,I., I+>¢kt;is. ,,\. and Porter, R. (1986) Short latency inpul, s It) phrcnic illt)ltHluill(llleS ii'11ill the scnsl)iin]otor cortex [i1 the c{it. I(xp. P,r;iiil I)xc.~. I~l: 2Sll 2qll. Mark~intl. ().IN.. Kincaid. J.('., P+,)Ul-lllalld. R.A., Moorthy, S.S., King. t<1.1)., M(ihanlc'ct, "l'. culd [+lrowi1, J.'~'. (1984) Electrophysiologic c\ahlclliOll ~)1 dial)hragm by tlan~.ctlt~ln~+'OtlS pt~renic nei~c stimu lillion. Nctlil>lo~_~, 34:6114 f~14. Mcrlon, I'.,.\. clnd ]MortolL l i B . (lt,iSl)) ,Stimulation of the cci-cbrill c'ltitcx in the intact htlnl{lll subject, N{ilui'e, 295: 277. NcwsOnl-l):lxis, .I.
2()7
Rohdc, V. and Zcntner. J. (1991) PrognoMic ;alu¢ ol motor evoked potentials in traumatic and nontraumatic ci)m;i. |it: Advances in Neurosurgery, vol. 19. Springcr-Verlag. Berlin. New York, pp. 194 20ft. Shielcls, C.B., Palohcimo, M.P.J., Backman. M.tt.. tLdmonds, I I.L. and Johnson, J.R. (1991)) |ntra~pctatixc use ol tianscranial magnetic m~tor evoked potentials. In: ('hokro;crt3, S. (t(d.), Magnctic Stimulation in Clinical Neurophysi~log~,. Butlcc, v(~rths. Boston London, pp. 173--184. Sinlihw~ski, T., Fleury, B., Laumois, S., ('alhala, t I.P., Bouchc, P. and Derennc. J.P. (Icj89) Cervical nlagnetic stinlulatinn: a new pain Icss method for bilateral phrenic neiac stimulatkm in ¢onsci~ms humans. ,I. AV,pl. Physiol., ~7(41:1311 131s. Swcnson. M R . and Rubcnstein. R.S. (l~,lc)21 Phrcnic nur\c comtuc lion studies. Muscle Ner¢c, 15:5~17 6113. Wiesncr. NIL. Sienlpien. L . M arid Maclcan. I.('. (19SN) Phrcnic ]lt.~i~.e conduction: The effect tH diaphragnmtic Disiti~m on the compound intlscl¢ aciioll polclllial. ]>il)cccdings o l the /\lllltlill Mucling o l the ,,\mcrican z\c~lclc'i/1~, iq Ph\sical Medicine :iilcl Rchahililalion, SCallle, X,VA, p 12t).