Acta Physiol Scand 1992, 146, 399-400
Changes in motor cortex excitability preceding voluntary ramp-and-hold plantarflexion in man J. N I E L S E N and N. P E T E R S E N Department of Neurophysiology, T h e Panum Institute, University of Copenhagen, Blegdamsvej 3 , 2200 Copenhagen N., Denmark
Techniques to activate descending tracts from the motor cortex to the spinal cord through the intact scalp in awake human subjects have recently appeared (Merton & Morton 1980, Barker et al. 1985). Whereas electric stimulation of the scalp apparently activates the descending axons directly, magnetic stimulation presumably activates the cortical cells indirectly or at the axon hillock (Day et al. 1989, Edgley e t al. 1990). Muscular responses evoked by magnetic stimulation consequently may be influenced by the excitability of the cortical cells. Indeed recently it has been demonstrated that the effect of magnetic stimulation of the motor cortex on spinal motoneuronal excitability (assessed by monosynaptic H-reflex testing) is taskdependent (Nielsen et al. 1993). During agonist contraction a facilitatory effect with a very short latency is thus observed, whereas an inhibition with a slightly longer latency is revealed by the same stimulus during antagonist contraction. These effects are presumably caused by activation of different sets of corticospinal cells reflecting their increased excitability in relation to specific tasks. In the present study it is demonstrated that the agonist-related early facilitation can be seen7&100 ms prior to the onset of contraction. The subjects (n = 7) were seated in an armchair with both feet attached to footplates which were connected to torque meters. The torque from both footplates was displayed as two dots on an oscilloscope in front of the subject (time base: 100 ms cm-'). The oscilloscope was triggered by a warning signal presented every 10 s. The subject's task was to make a plantarflexion of both feet in response to the signal so as to superimpose the two dots on ramps drawn on the oscilloscope (onset 400 ms after the warning signal, a duration of 300 ms and an amplitude of 5 Nm). conditioned (with magnetic stimulation of the cortex; Received 18 June 1992, accepted 4 August 1992. Key words: H-reflex, magnetic stimulation, motoneurones, motor cortex. Correspondence: J. Nielsen, Department of Neurophysiology, The Panum Institute, University of Copenhagen, Blegdamsvej 3, 2200 Copenhagen N., Denmark.
see below) and control H-reflexes (without magnetic stimulation) were elicited in the right soleus muscle by a single electrical stimulus to the posterior tibia1 nerve in the fossa poplitea at different timings in relation to the warning signal. The latency of the reflexes in relation to the voluntary EMG was subsequently calculated off-line trial by trial. In intermingled trials without stimulation the onset of EMG in the two soleus muscles was found to be very similar and the onset of the EMG in the left muscle could consequently be used to facilitate the determination of the true EMG-onset in the right muscle during the silent period in the EMG following the H-reflex. The size of the reflexes was measured from the surface EMG as the peak-to-peak amplitude and expressed as a percentage of the maximal direct motor
.
. 0
0 0
-150
-115
.
-too
O
-75
0
O
-60
-15
0
IS
50
7,
(00
115
Time b e f o r e o n s e t of E M G - a c t i v i t y (ms)
Fig. 1. The size of the conditioned ( 0 )and control (0) soleus H-reflex at different times in relation to the onset of voluntary EMG in the soleus muscle. The Hreflex was conditioned by a magnetic stimulation of the motor cortex at an interval of - 3 ms (the test reflex preceded the conditioning magnetic stimulation) and with an intensity of 45%. The size of the at rest is conditioned (A)and control reflexes (A) shown to the right in the figure. The responses are expressed as a percentage of M,,,. Each point represents the average of 5-15 reflex measurements.
399
400
3. AYielsenand
>V.Petersen
response following supramaximal stimulation (cortico-motoneurnal cells) begin to fire about 100 ms of the posterior tibia1 nerve. The reflexes were prior to the onset of contraction (Cheney & Fetz 1980), thus very similar to the onset of the facilitation conditioned b!- a magnetic stimulation of the motor cortex (Magstim model 200 stimulator, The Slagstim in relation to the E M G in the present study. We Company Limited, England). The centre of the suggest that the increase of the control reflexes 40-70 stimulating double-cone coil was placed 2 cm lateral rns prior to the movement reflects an increased and 2 cm posterior to the 1-ertex. The intensit!. of the excitabilit!- of motoneurones, whereas the increase of stimulation a a s expressed a5 a percentage of the the conditioned reflex 20-30 ms in advance reflects maximal output of the stimulator. In the beginning of the increased excitability of cortico-motoneuronal each experiment the intensit!. was adjusted so that it cells. T h e results consequently suggest that the present experimental paradigm allows to study the excitability was below the threshold for eliciting an evoked of popzrlntions of cortico-motoneuronal cells in the potential in the soleus muscle even during strong human cortex thus supplementing chronic single unit plantarflexion. A time course of the effect of the recordings in monkey. magnetic stimulation on the H-reflex was then obtained during a tonic plantarflexion. In order to Supported by the Danish Health Research Council, study the excitabilit!- of those cortical neurones that the Society of Multiple Sclerosis, the Lundbeck project directly to soleus motoneurones the earliest Foundation and the Lauridts Petersen Foundation. possible conditioning-test inter\-al for which a facilitation could be seen \$-as used for the rest of the R E F E R E N C E S experiment. Conditioned (with the magnetic stimu1.L. 1985. lation) and control (without magnetic stimulation) B4RKER, -4.T.,JALINOUS, R. & FREESTON, Non-invasive magnetic stimulation of the human reflexes were randomly alternated in series of .iO motor cortex. Luncet ii, 110&1107. measurements. In Figure I is presented the size of the control (0)CHENE\-,P.D. & FETZ,E.E. 1980. Functional classes of primate corticomotoneuronal cells and their and conditioned soleus H-reflex ( 0 )at different times relation to active force. 3Neuropllysrol44, 773-791. in relation to the onset of Yoluntar!- EllG-activity in DAY,B.L., DRESSLER, D., MAERTENS DE NOORDHOUT, the soleus muscle. The intensity of the test stimularion -I., RIARSDEN, C.D., NAKASHIMA, K., ROTHWELL, as adjusted to obtain an H-reflex at rest of .To,, of J.C. & THOMPSON, P. 1989. Electric and magnetic Xi,,).,\ In this situation the magnetic stimulation stimulation of human motor cortex: surface E M G was kept so low (intensit!. 4 5 O , , ; conditioning-test and single motor unit responses. 3 Ph,ysiul 412, InterI-al - 3 ms) as to have no effect on the H-reflex. 449-473. ;it latencies longer than 100 ms prior to the ESIGEDGLE\-, S.A., EYRE,J.A., LEMON, R.N. & MILLER,S. onset control and conditioned reflexes had the same 1990. Excitation of the corticospinal tract by size as a t rest. At latencies 90-100 ms prior to the electromagnetic and electrical stimulation of the onset of contraction the conditioned reflexes, however, scalp in the macaque monkey. 3 Physiol, 425, increased signiticantl!- in size, whereas control reflexes 301-320. did not increase until 61t70 ms prior to the ESIG. I n ~ I E R T POAN. ,& MORTON,H.B. 1980. Stimulation of the cerebral cortex in the intact human subject. the other six subjects control reflexes increased 4%70 .V(iture 285, 225. m5 prior to the E.1lG, iyhereas conditioned reflexes SIELSF.N, J., PETERSEN, N.& DEUSCHL, G. 1993. Task increased 20-30 rns earlier. related changes in the effect of magnetic brain In primates, cells in the motor cortex n.ith direct stimulation in man.JPh.ysiol459 (Oxford Phy. Soc. monos!-naptic projections to the motoneurones Xleeting, 27-29 July 1992).
(a).
Changes in motor cortex excitability preceding voluntary ramp-and-hold plantarflexion in man J. N I E L S E N and N. P E T E R S E N Department of Neurophysiology, T h e Panum Institute, University of Copenhagen, Blegdamsvej 3 , 2200 Copenhagen N., Denmark
Techniques to activate descending tracts from the motor cortex to the spinal cord through the intact scalp in awake human subjects have recently appeared (Merton & Morton 1980, Barker et al. 1985). Whereas electric stimulation of the scalp apparently activates the descending axons directly, magnetic stimulation presumably activates the cortical cells indirectly or at the axon hillock (Day et al. 1989, Edgley e t al. 1990). Muscular responses evoked by magnetic stimulation consequently may be influenced by the excitability of the cortical cells. Indeed recently it has been demonstrated that the effect of magnetic stimulation of the motor cortex on spinal motoneuronal excitability (assessed by monosynaptic H-reflex testing) is taskdependent (Nielsen et al. 1993). During agonist contraction a facilitatory effect with a very short latency is thus observed, whereas an inhibition with a slightly longer latency is revealed by the same stimulus during antagonist contraction. These effects are presumably caused by activation of different sets of corticospinal cells reflecting their increased excitability in relation to specific tasks. In the present study it is demonstrated that the agonist-related early facilitation can be seen7&100 ms prior to the onset of contraction. The subjects (n = 7) were seated in an armchair with both feet attached to footplates which were connected to torque meters. The torque from both footplates was displayed as two dots on an oscilloscope in front of the subject (time base: 100 ms cm-'). The oscilloscope was triggered by a warning signal presented every 10 s. The subject's task was to make a plantarflexion of both feet in response to the signal so as to superimpose the two dots on ramps drawn on the oscilloscope (onset 400 ms after the warning signal, a duration of 300 ms and an amplitude of 5 Nm). conditioned (with magnetic stimulation of the cortex; Received 18 June 1992, accepted 4 August 1992. Key words: H-reflex, magnetic stimulation, motoneurones, motor cortex. Correspondence: J. Nielsen, Department of Neurophysiology, The Panum Institute, University of Copenhagen, Blegdamsvej 3, 2200 Copenhagen N., Denmark.
see below) and control H-reflexes (without magnetic stimulation) were elicited in the right soleus muscle by a single electrical stimulus to the posterior tibia1 nerve in the fossa poplitea at different timings in relation to the warning signal. The latency of the reflexes in relation to the voluntary EMG was subsequently calculated off-line trial by trial. In intermingled trials without stimulation the onset of EMG in the two soleus muscles was found to be very similar and the onset of the EMG in the left muscle could consequently be used to facilitate the determination of the true EMG-onset in the right muscle during the silent period in the EMG following the H-reflex. The size of the reflexes was measured from the surface EMG as the peak-to-peak amplitude and expressed as a percentage of the maximal direct motor
.
. 0
0 0
-150
-115
.
-too
O
-75
0
O
-60
-15
0
IS
50
7,
(00
115
Time b e f o r e o n s e t of E M G - a c t i v i t y (ms)
Fig. 1. The size of the conditioned ( 0 )and control (0) soleus H-reflex at different times in relation to the onset of voluntary EMG in the soleus muscle. The Hreflex was conditioned by a magnetic stimulation of the motor cortex at an interval of - 3 ms (the test reflex preceded the conditioning magnetic stimulation) and with an intensity of 45%. The size of the at rest is conditioned (A)and control reflexes (A) shown to the right in the figure. The responses are expressed as a percentage of M,,,. Each point represents the average of 5-15 reflex measurements.
399
400
3. AYielsenand
>V.Petersen
response following supramaximal stimulation (cortico-motoneurnal cells) begin to fire about 100 ms of the posterior tibia1 nerve. The reflexes were prior to the onset of contraction (Cheney & Fetz 1980), thus very similar to the onset of the facilitation conditioned b!- a magnetic stimulation of the motor cortex (Magstim model 200 stimulator, The Slagstim in relation to the E M G in the present study. We Company Limited, England). The centre of the suggest that the increase of the control reflexes 40-70 stimulating double-cone coil was placed 2 cm lateral rns prior to the movement reflects an increased and 2 cm posterior to the 1-ertex. The intensit!. of the excitabilit!- of motoneurones, whereas the increase of stimulation a a s expressed a5 a percentage of the the conditioned reflex 20-30 ms in advance reflects maximal output of the stimulator. In the beginning of the increased excitability of cortico-motoneuronal each experiment the intensit!. was adjusted so that it cells. T h e results consequently suggest that the present experimental paradigm allows to study the excitability was below the threshold for eliciting an evoked of popzrlntions of cortico-motoneuronal cells in the potential in the soleus muscle even during strong human cortex thus supplementing chronic single unit plantarflexion. A time course of the effect of the recordings in monkey. magnetic stimulation on the H-reflex was then obtained during a tonic plantarflexion. In order to Supported by the Danish Health Research Council, study the excitabilit!- of those cortical neurones that the Society of Multiple Sclerosis, the Lundbeck project directly to soleus motoneurones the earliest Foundation and the Lauridts Petersen Foundation. possible conditioning-test inter\-al for which a facilitation could be seen \$-as used for the rest of the R E F E R E N C E S experiment. Conditioned (with the magnetic stimu1.L. 1985. lation) and control (without magnetic stimulation) B4RKER, -4.T.,JALINOUS, R. & FREESTON, Non-invasive magnetic stimulation of the human reflexes were randomly alternated in series of .iO motor cortex. Luncet ii, 110&1107. measurements. In Figure I is presented the size of the control (0)CHENE\-,P.D. & FETZ,E.E. 1980. Functional classes of primate corticomotoneuronal cells and their and conditioned soleus H-reflex ( 0 )at different times relation to active force. 3Neuropllysrol44, 773-791. in relation to the onset of Yoluntar!- EllG-activity in DAY,B.L., DRESSLER, D., MAERTENS DE NOORDHOUT, the soleus muscle. The intensity of the test stimularion -I., RIARSDEN, C.D., NAKASHIMA, K., ROTHWELL, as adjusted to obtain an H-reflex at rest of .To,, of J.C. & THOMPSON, P. 1989. Electric and magnetic Xi,,).,\ In this situation the magnetic stimulation stimulation of human motor cortex: surface E M G was kept so low (intensit!. 4 5 O , , ; conditioning-test and single motor unit responses. 3 Ph,ysiul 412, InterI-al - 3 ms) as to have no effect on the H-reflex. 449-473. ;it latencies longer than 100 ms prior to the ESIGEDGLE\-, S.A., EYRE,J.A., LEMON, R.N. & MILLER,S. onset control and conditioned reflexes had the same 1990. Excitation of the corticospinal tract by size as a t rest. At latencies 90-100 ms prior to the electromagnetic and electrical stimulation of the onset of contraction the conditioned reflexes, however, scalp in the macaque monkey. 3 Physiol, 425, increased signiticantl!- in size, whereas control reflexes 301-320. did not increase until 61t70 ms prior to the ESIG. I n ~ I E R T POAN. ,& MORTON,H.B. 1980. Stimulation of the cerebral cortex in the intact human subject. the other six subjects control reflexes increased 4%70 .V(iture 285, 225. m5 prior to the E.1lG, iyhereas conditioned reflexes SIELSF.N, J., PETERSEN, N.& DEUSCHL, G. 1993. Task increased 20-30 rns earlier. related changes in the effect of magnetic brain In primates, cells in the motor cortex n.ith direct stimulation in man.JPh.ysiol459 (Oxford Phy. Soc. monos!-naptic projections to the motoneurones Xleeting, 27-29 July 1992).
(a).
