Contralateral influences on triceps surae motoneuron excitability

Electroencephalography and clinical Neurophysiology , 85 (1992) 177-182 © 1992 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/92/$05.00

177

ELMOCO 91075

C o n t r a l a t e r a l i n f l u e n c e s on triceps surae m o t o n e u r o n excitability David M. Koceja

a

and Gary Kamen b

a Motor Control Laboratory, Department of Kinesiology, Indiana University, Bloomington, IN 47405 (U.S.A.), and ~ Departments of Physical Therapy and Health Sciences, Boston University, Boston, MA 02215 (U.S.A.) (Accepted for publication: 19 October 1991)

Summary In an effort to more fully investigate spinal reflex pathways in humans, we measured the isometric force-time curve of the tibial nerve H-reflex in 12 college age subjects. We also conditioned the reflex with a contralateral H-reflex stimulus or a contralateral tendon-tap, to ascertain the effects of crossed spinal segmental inputs on alpha motoneuron excitability. The conditioning stimulus preceded the test reflex by 10, 25, 40, 55, 70, 85, 100, 115, 130 or 145 msec. The results demonstrate that a conditioning tibial nerve H-reflex produced marked facilitation onto the contralateral triceps surae motoneurons, predominantly at longer-latency intervals. Conversely, a conditioning Achilles tendon-tap produced long-latency inhibition to the triceps surae. These results demonstrate that differential motoneuron excitability changes can be produced by electrical and mechanical conditioning stimuli. Moreover, these excitability changes may be long lasting and only appear after a relatively long latency. Several neurophysiological mechanisms are proposed to contribute to these changes. Key words: H-reflex; Conditioned reflexes; Recovery curve; (Human)

Conditioning protocols have been successfully used in the past to define the role of segmental inputs on alpha motoneuron excitability. For example, conditioning a test H-reflex by a preceding subliminal H-reflex stimulus in the ipsilateral limb produces a well defined recovery profile of inhibition to the triceps surae motoneurons (Paillard 1959). A similar conditioning stimulus to the contralateral limb, however, produces facilitation to the triceps surae motoneurons (Robinson et al. 1979). The combined influences of cutaneous receptor activation (type III fibers) and long-loop reflexes (Tabo~fkovfi and Sax 1969; Gassel and Ott 1970) have been suggested as responsible mechanisms mediating these motoneuron excitability changes. When examining the mechanical tendon-tap reflex, it has been demonstrated that crossed spinal mechanical conditioning produces long-latency inhibition to the triceps surae and long-latency facilitation to the quadriceps muscles (Koceja and Kamen 1991). These effects have been shown to persist for up to 150 msec (Koceja and Kamen 1988; Koceja et al. 1990), and to be different for trained subject groups and the elderly (Kamen and Koceja 1989; Koceja et al. 1991; Koceja and Kamen 1992). Whereas the exact mechanisms responsible for such reported motoneuron excitability changes have yet to

Correspondence to: David M. Koceja, Ph.D., HPER 170, Indiana University, Bloomington, IN 47405 (U.S.A.).

be addressed, a conditioning paradigm provides a useful means of documenting the time course of such changes. One possible explanation for the differences observed in H- and tendon-reflex studies may be the spatial and temporal effects produced by the conditioning stimulus, as well as the possible differences in cutaneous receptor activation (Schieppati 1987). H-reflexes may activate the largest diameter sensory fibers, and one might also speculate that their effects at the motoneuron pool may be different from that produced by the Ia and other afferences activated by the mechanical tendon-tap. The purpose of this study was to examine human triceps surae excitability following a conditioning stimulus to the contralateral limb. By examining the reflex recovery profile of the tibial nerve H-reflex conditioned by a mechanical or an electrical stimulus, the role that the characteristics of the conditioning stimulus have on motoneuron excitability could be ascertained. Also, it was the purpose of this study to examine the crossed spinal connections mediating the human triceps surae muscles.

Methods

Data were obtained from 12 subjects (mean age = 28.4 years) who read and signed a subject informed consent form. These individuals were drawn from a healthy population with no apparent neurological, or-

178 thopedic or neuromuscular problems. During testing, the subject sat on a modified Elgin table. The subject wore opaque goggles to prevent visual input and listened to soothing music through headphones to prevent anticipatory responses. The test reflex was a 50% maximal H-reflex. The stimulating electrodes were placed longitudinally in the popliteal fossa along the tibial nerve. A 1 msec square wave pulse (Grass Model $44) was delivered to elicit a maximal H-reflex free of any direct M-response. The stimulus intensity was then reduced to elicit a 50% max peak-to-peak amplitude H-reflex. Two experimental treatments were randomly assigned to each subject: (1) the right leg tibial nerve H-reflex was conditioned by a contralateral tibial nerve H-reflex (50% max); and (2) the right leg tibial nerve H-reflex was conditioned by a tap to the contralateral Achilles tendon. The conditioning stimulus preceded the test reflex by 10, 25, 40, 55, 70, 85, 100, 115, 130 or 145 msec. Control responses, in which the tibial nerve H-reflex was elicited in the right leg with no preceding conditioning stimulus, were also obtained. Changes in test reflex excitability were determined by examining both electromyographic and force-time characteristics of the reflex response. The isometric force output of the reflex response was recorded with a loadcell (Dillon Corp., model Z). An electromagnetic solenoid was used to deliver the conditioning tendontaps. Connected in series with the solenoid was a piezoelectric force transducer, which was used to monitor the force of each tendon-tap, to ensure that identical taps were delivered on each trial. Bipolar recording electrodes of 1 cm diameter were positioned over the soleus muscle, approximately 4 cm above the point where the two heads of the gastrocnemius join the Achilles tendon. Electrodes were placed longitudinally at the midline of the leg. A 2 cm intraelectrode distance was used, with the ground electrode positioned midway between the two recording electrodes. The signals from the transducer, the load cell and the surface electrodes were amplified and interfaced with an IBM computer equipped with a data acquisition board (Data Translation, Model DT-2801a). Sampling rate for data collection purposes was set at 2 kHz. On each trial, the following dependent measures were recorded: peak isometric force (PF), electromechanical delay (EMD - the time in msec between the beginning of E M G activity until the initial deflection of force), peak-to-peak E M G activity, contraction time (CT) and half-relaxation time (1/2-RT). For each dependent variable, a 2 x 11 (condition X interval) A N O V A was used to determine whether the conditioning stimulus produced any changes in the test reflex. When significant differences across conditioning intervals were found, the Dunnett's post-hoc test was

D.M. KOCEJA, G. KAMEN TABLE I lntraclass reliability (trial-by-trial) coefficients for peak isometric force and peak-to-peak EMG activity for the two experimental conditions. Conditioning stimulus H-reflex Tendon-tap

Peak force 0.95 0.93

Peak-to-peakEMG 0.90 0.89

used to isolate at which specific intervals the changes occurred. Polynomial trend analyses across conditioning intervals were also used to describe the reflex recovery profile of each experimental condition. For all statistical tests, an alpha level of 0.05 was used.

Results To determine whether the dependent measures were consistent from trial to trial, reliability coefficients were calculated. A subject × trial A N O V A model was used to isolate the variability due to subjects and trials. Trial-by-trial correlation coefficients (Kirk 1982)were then calculated to estimate the trial-to-trial consistency. For peak force and peak to peak E M G activity at the unilateral condition, all reliability estimates were 0.89 or greater (Table I) indicating highly consistent results from trial to trial.

Contralateral tibial nerve When the tibial nerve H-reflex was conditioned by a contralateral tibial nerve H-reflex, a long-latency facilitation was observed. The unilateral control value of 23.3 N was markedly facilitated at the 85 (31.1 N), 100 (32.1 N) and 115 msec (32.7 N) intervals. A similar trend was noted for peak-to-peak E M G activity, and the group data are shown in Fig. 1. For the group, maximal facilitation occurred at the 100 msec interval when peak force was enhanced by 40.3% and peak-topeak E M G activity was 26.2% above the control value. The analysis of the recovery profile for peak force showed a significant linear trend, accounting for 52.2% of the variability in the data. No significant changes were noted for contraction time although the tendency was for these values to be lengthened throughout the conditioning trials, as shown in Fig. 1D. Similarly, electromechanical delay (Fig. 1C) displayed a tendency to be lengthened throughout the conditioning intervals as did half-relaxation time (Fig. 1E). Contralateral tendon-tap When the tibial nerve H-reflex was conditioned by a contralateral tendon-tap, a quite different recovery profile was displayed. The mechanical stimulus produced a significant inhibition to the triceps surae. Again the conditioning effect was most evident at the

C O N T R A L A T E R A L I N F L U E N C E S ON TRICEPS SURAE

40-

179

PEAK FORCE

2.00

T B.

PEAKTO PEAK EMG

35-

~1.25

U~ 30. Z

~

25.

Z

20, 15, 10

I

I

C

26 01 z

I

I

25

I

I

55

I

I

I

B5

115

CONDITIONING I ~ N .

(MS)

I

! ! t

1

t C

145

140.

C. ELEC/ROMECHANIC/¢DELAY

24

I

I

I

I

I

I

I

I

I

25 55 85 115 CONDmONING INI,':.dVAL (MS~

I

I

145

D. CONTRACTIONTIME

130,

22

~

120,

01

-i 2o 110,

1B 16

I C

110

I

I

I

25

I

I

55

I

I

I

B5

115

CONDITIONING I ~ A L

(MS)

I

I

I

145

90

I

I

C

I

25

I

I

55

I

I

85

I

I

115

I

I

145

CONDFIIONING INTERVAL (MS)

E. HALF-RELAXATIONTIME

1O0 U') CI Z o 90

LEGEND

VI

I1~111 e~e

H-REFLEX TENDON-TAP

70" 6C

I C

I

I

25

I

I

55

I

I

B5

I

I

115

I

I

14,5

CONDmONING INTERVAL (MS) Fig. 1. Reflex recovery profiles depicting: H-reflex - tibial nerve H-reflex conditioned by a contralateral tibial nerve H-reflex; and tendon-tap tibial nerve H-reflex conditioned by a contralateral Achilles tendon-tap. Data are pooled across all subjects. C represents the unilateral control value. Data are smoothed with a cubic spline routine.

longer-latency intervals. Peak force was reduced at the 55 (15.7 N), 70 (15.1 N), 100 (16.6 N) and 115 msec (16.2 N) intervals when compared with the control value. The group results are contrasted with the tibial nerve conditioning results in Fig. 1. Maximal inhibition for peak force occurred at the 70 msec interval, when force output was 64.8% of the control value. The recovery profile for peak force was characterized by a significant linear (35.6%) and quadratic (31.2%) trend. From Fig. 1A, the 2 phases of recovery can be seen: an initial and steep depression between the 25 and 70

msec intervals, followed by a consistent level depression between the 70 and the 145 msec intervals. For the group, no changes were noted for electromechanical delay (Fig. 1C), contraction time (Fig. 1D) or halfrelaxation time (Fig. 1E), although electromechanical delay displayed a lengthening and contraction time displayed a shortening during the conditioning intervals. The contrast between the two conditions can be seen for a typical subject in Fig. 2. It can be seen that as the conditioning interval was lengthened, the crossed

180

D.M. KOCEJA, G. KAMEN H-REFLEX

70

ms

100

ms

130

ms

l

I I

. . . .

TENDON-TAP

I I

. . . .

i

. . . .

L

_

_ 50

I

l

. . . .

J

. . . .

i

. . . .

i

J ms

Fig. 2. Raw data of a typical subject depicting the E M G records at the 40, 70, 100 and 130 msec conditioning intervals. H-reflex trace depicts the 50% maximum tibia] nerve H-reflex conditioned by a contralateral 50% maximum tibia] nerve H-reflex. Tendon-tap trace depicts the 50% maximum tibial nerve H-reflex conditioned by a contralatera] Achilles tendon-tap. Note the different responses of triceps surae to the two conditioning stimuli: long-latency facilitation results from electrical conditioning, and long-latency inhibition results from mechanical conditioning.

spinal H-reflex stimulus produced a marked facilitation whereas the crossed spinal mechanical stimulus produced marked inhibition at the same intervals.

Discussion

The notion that spinal mechanisms can regulate centrally programmed movements was first introduced by Sherrington (1910), and it is well documented that there exists a bilateral coordination in man. For example, gating at the spinal cord, resulting in reflex switching during locomotion, has been demonstrated (Grillner 1975). Also, postural perturbations can be shown to inhibit or facilitate the reflex system (Nashner 1976). During stance, unilateral displacements of one leg produces a bilateral response with similar latencies on

both sides (Dietz and Berger 1984; Berger et al. 1987). In addition, unilateral perturbations during gait are known to be followed by a bilateral EMG response. Because of the short latency of these responses, it has been suggested that they take place at the spinal level (Dietz et al. 1989). The present results indicate that bilateral conditioning produces marked changes in motoneuron excitability. The present type of analysis is useful in examining the exact interactions of spinal pathways. The results of this study demonstrate that motoneuron excitability is enhanced by a crossed spinal electrical conditioning stimulus whereas a mechanical stimulus produces crossed spinal inhibition to the triceps surae. The data from this study, in which an electrical conditioning stimulus produces long-latency excitation to the contralateral limb, are consistent with previous results (Robinson et al. 1979). Robinson et al. (1979) reported maximal facilitation at the 150 msec interval when conditioning with a subliminal H-reflex stimulus. These results suggest a similar latency and effect when using a 50% maximal H-reflex as the conditioning reflex. The magnitude of the conditioning effect was slightly greater in the Robinson et al. (1979) study, although they utilized a 20% test reflex. In the present study the test reflex was a 50% maximal reflex. Near maximal test H-reflexes are much less likely to exhibit facilitation than are submaximal test responses (Clare and Landau 1964; Gassel and Diamantopoulos 1964), which would account for the slightly less amount of facilitation caused by the contralateral conditioning stimulus in the present study. Increases in motoneuron excitability caused by the crossed spinal conditioning could result from several mechanisms. In both young and old adults, input from skin receptors overlying ipsilateral and contralateral calf and anterior thigh regions facilitates the patellar tendon reflex (Burke et al. 1989). Similarly, Gassel and Ott (1970, 1973) have demonstrated a long-latency facilitation of the patellar tendon reflex following cutaneous stimulation to various skin areas. Similarly, Hultborn et al. (1987) reported that in a small percentage of subjects, contralateral tendon vibration resulted in long-latency (100-140 msec) facilitation to the soleus muscle. Moreover, the use of local anesthetics eliminated this facilitation, supporting the role of cutaneous receptors in mediating these effects. It is also documented that mechanically induced afferent volleys activate oligosynaptic pathways in man, since these volleys are contaminated by a variety of afferents from a variety of sources (Burke et al. 1984). Similarly, group Ib inhibition (Pierrot-Deseilligny et al. 1981b), as well as cutaneous depression (Pierrot-DeseiIligny et al. 1981a) and facilitation (Bergego et al. 1981) of Ib inhibition have been demonstrated to be mediated by the activity of spinal interneurons.

CONTRALATERAL INFLUENCES ON TRICEPS SURAE

Previous reports have demonstrated that a weak and short-lasting vibration applied to the skin above the tibialis anterior muscle caused an inhibition of the soleus H-reflex which lasted 250 msec (Morin et al. 1984). Hultborn et al. (1987) also demonstrated an early (25 msec) facilitation and late inhibition (40-300 msec) (their Fig. 4C) of the soleus H-reflex as a result of such tendon vibration. The results from this study (Fig. 1A) demonstrate an identical profile. Hultborn et al. speculated that the early facilitation was due to the spread of the vibration to soleus muscle spindles, thereby causing homonymous Ia EPSPs in soleus motoneurons. In terms of the long-latency inhibition, local anesthetics failed to alter the profile. The long-latency inhibition, therefore, was attributed to presynaptic mechanisms rather than cutaneous effects (Hultborn et al. 1987). It is interesting to speculate that a similar mechanism is operative in the present paradigm, as the vibratory tendon-tap stimulus may produce similar, bilateral effects on the system. This is intriguing to speculate as the degree of facilitation and inhibition is reduced in the bilateral condition. For example, the maximal facilitation in the Hultborn et al. (1987) study was approximately 45% whereas the bilateral results in this study suggest 16%. Similarly, the maximal longlatency effects in the Hultborn et al. (1987) study was approximately 50% at the 50 msec interval, whereas in this study it was 37% at the 70 msec interval. Certainly, another logical candidate might involve supraspinal influences acting upon the reflex arc. There are a number of possible pathways, and these include propriospinal (Faganel and Dimitrijevi6 1982), spinobulbo-spinal (Meier-Ewert et al. 1972), rubrospinal (Shieh et al. 1985) and corticospinal (Wiesendanger 1969) connections. Again, however, the close correspondence between our data and those of Hultborn et al. leads one to believe that spinal mechanisms are responsible.

ConcLusion

It is concluded that differential excitability changes result from crossed spinal conditioning of the H-reflex. Moreover, a wave of long-latency inhibition exists when the conditioning stimulus is a mechanical tendon-tap, whereas a wave of long-latency excitation exists when the conditioning stimulus is an electrical H-reflex. It is speculated that the facilitation to the contralateral limb caused by the H-reflex stimulus is mediated by cutaneous receptors, whereas the long-latency inhibition produced by tendon-tap stimulus is mediated by presynaptic mechanisms. However, the exact mechanisms and their functional implications remain to be determined.

181

References Bergego, C., Pierrot-Deseilligny, E. and Mazi?~res, L. Facilitation of transmission in Ib pathways by cutaneous afferents from the contralateral foot sole in man. Neurosci. Lett., 1981, 27: 297-301. Berger, W., Dietz, V. and Horstmann, G. Interlimb coordination of posture in man. J. Physiol. (Lond.), 1987, 390: 135. Burke, D., Gandevia, S.C. and McKeon, B. Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J. Neurophysiol., 1984, 52: 435-448. Burke, J.R., Kamen, G. and Koceja, D.M. Long-latency enhancement of quadriceps excitability from stimulation of skin afferents in young and old adults. J. Gerontol., 1989, 44: M158-M163. Clare, M.H. and Landau, W.M. Fusimotor function. Part V. Reflex reinforcement under fusimotor block in normal subjects. Arch. Neurol., 1964, 10: 123-127. Dietz, V. and Berger, W. Inter-limb coordination of posture in patients with spastic paresis: impaired function of spinal reflexes. Brain, 1984, 107: 965-978. Dietz, V., Horstmann, A. and Berger, W. Interlimb coordination of leg-muscle activation during perturbation of stance in humans. J. Neurophysiol., 1989, 62: 680-693. Faganel, J. and Dimitrijevi6, M.R. Study of propriospinal interneuron system in man. J. Neurol. Sci., 1982, 56: 155-172. Gassel, M.M. and Diamantopoulos, E. The Jendrassik maneuver. II. An analysis of the mechanism. Neurology, 1964, 14: 640-642. Gassel, M.M. and Ott, K.H. Local sign and late effects on motoneuron excitability of cutaneous stimulation in man. Brain, 1970, 93: 95-106. Gassel, M.M. and Ott, K.H. Patterns of reflex excitability change after widespread cutaneous stimulation in man. J. Neurol. Neurosurg. Psychiat., 1973, 36: 282-287. Grillner, S. Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol. Rev., 1975, 55: 247-304. Hultborn, H., Meunier, S., Morin, C. and Pierrot-Deseilligny, E. Assessing changes in presynaptic inhibition of Ia fibres: a study in man and cat. J. Physiol. (Lond.), 1987, 389: 729-756. Kamen, G. and Koceja, D.M. Contralateral influences on patellar tendon reflexes in young and old adults. Neurobiol. Aging, 1989, 10: 311-315, Kirk, R.E. Experimental Design: Procedures for the Behavioral Sciences. Brooks/Cole Publishing, Belmont, CA, 1982. Koceja, D.M. and Kamen, G. Conditioned patellar tendon reflexes in sprint- and endurance-trained athletes. Med. Sci. Sports Exerc., 1988, 20: 172-177. Koceja, D.M. and Kamen, G. Interactions of human quadriceps-triceps-surae motoneuron pathways. Exp. Brain Res., 1991, 86: 433-439. Koceja, D.M. and Kamen, G. Segmental reflex organization in endurance-trained and untrained subjects. Med. Sci. Sport Exerc., 1992, 24: 235-241. Koceja, D.M., Burke, J.R. and Kamen, G. Quadriceps excitability is enhanced by a conditioning tap to the Achilles tendon. Electromyogr. Clin. Neurophysiol., 1990, 30: 415-421. Koceja, D.M., Burke, J.R. and Kamen, G. Organization of segmental reflexes in trained dancers. Int. J. Sports Med., 1991, 12: 285-289. Meier-Ewert, K., Humme, U. and Dahm, J. New evidence favouring long loop reflexes in man. Arch. Psychiat. Nervenkr., 1972, 215: 121-128. Morin, C., Pierrot-Deseilligny, E. and Hultborn, H. Evidence for presynaptic inhibition of muscle spindle Ia afferents in man. Neurosci. Lett., 1984, 44: 137-142. Nashner, L.M. Adapting reflexes controlling the human posture. Exp. Brain Res., 1976, 26: 59-72. Paillard, J. Functional organization of afferent innervation of muscle studied in man by monosynaptic testing. Am. J. Phys. Med., 1959, 38: 239-247.

182 Pierrot-Deseilligny, E., Bergego, C., Katz, R. and Morin, C. Cutaneous depression of Ib pathways to motoneurones in man. Exp. Brain Res., 1981a, 42: 351-361. Pierrot-Deseilligny, E., Morin, C., Bergego, C. and Tankov, N. Pattern of group I fibre projections from ankle flexor and extensor muscles in man. Exp. Brain Res., 1981b, 42: 337-350. Robinson, K.L., McIIwain, J.S. and Hayes, K.C. Effects of H-reflex conditioning upon the contralateral alpha motoneuron pool. Electroencepb. clin. Neurophysiol., 1979, 46: 65-71. Schieppati, M. The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog. Neurobiol., 1987, 28: 345-376.

D.M. KOCEJA, G. KAMEN Sherrington, C.S. Flexion reflex of the limb, crossed-extension reflex, and reflex stepping and standing. J. Physiol. (Lond.), 1910, 40: 28-121. Shieh, J.Y., Leong, S.K. and Wong, W.C. Effect of spinal cord hemisection on rubrospinal neurons in the albino cat. J. Anat. (Lond.), 1985, 143: 129-141. Tabo~ikov~, H. and Sax, D.S. Conditioning of H-reflexes by a preceding subthreshold H-reflex stimulus. Brain, 1969, 92: 203-212. Wiesendanger, M. The pyramidal tract: recent investigations on its morphology and function. Ergebn. Physiol., 1969, 61: 71-136.