Yasuhiro Kagamihara

Disorder in reciprocal innervation upon initiation of voluntary movement in patients with Parkinson's disease

SummaryReciprocal innervation of the soleus motoneurones upon initiation of voluntary ankle dorsiflexion was investigated in eight patients with Parkinsons disease. H-reflex and visually guided step tracking methods were used for testing moto-neurone excitability and for controlling the timing of movement initiation, respectively. While reciprocal inhibition appeared almost simultaneously with the agonist electromyographic (EMG) onset in normal subjects (Kagamihara and Tanaka 1985), facilitation appeared in the majority of patients under the same onset condition. It increased slowly, reaching a maximum at about 100 ms after the EMG onset. It then subsided slowly at around 200–300 ms, and was replaced thereafter by an inhibitory effect. No coactivation of the soleus muscle was detected electromyographically. The facilitation between the EMG onset and the onset of mechanical contraction was attributed to the direct effect of the descending command from the brain, suggesting a certain disorder in controlling the system for reciprocal innervation.

Reciprocal inhibition upon initiation of voluntary movement.

Phasic changes in reciprocal inhibition of the soleus motoneurons upon initiation of active ankle dorsiflexion was investigated in normal man. H-reflex and reaction time methods were combined. Two phases of reciprocal inhibition were observed. The first inhibition appeared almost simultaneously with the activity of agonist EMG but was so weak as to be cancelled with a strong test stimulus or a slight stretch of the test muscle. The second inhibition developed 100 ms after EMG onset, in the early stage of dynamic contraction, and was strong. These inhibitions increased as the voluntary effort was strengthened. The neural mechanism of these inhibitions is discussed.

Excitability of spinal inhibitory circuits in patients with spasticity.

The excitability of Ia inhibition and D1 inhibition after stimulation of the common peroneal nerve to the soleus motoneuron pool was investigated in 37 spastic patients at rest and onset of voluntary ankle dorsiflexion. Ia inhibition was determined as the short-latency depression of the soleus H-reflex and D1 inhibition as the long-latency depression. There was no significant difference in Ia inhibition between the paraplegic and control groups, however Ia inhibition in the hemiplegic group was significantly decreased. D1 inhibition was reduced in the paraplegic and hemiplegic groups compared with controls. Although inhibition of the soleus H-reflex appeared at the onset of voluntary dorsiflexion in control subjects, it was not observed in the patients. Although the excitability of the Ia inhibitory pathway at rest in the patients did not differ from that in control subjects, facilitation of the Ia inhibitory pathway at the onset of movement was decreased in the patients. Ia inhibition and D1 inhibition were evaluated in two paraplegic patients who were treated with local anesthesia and surgery, respectively. The excitability of both inhibitory pathways at rest was unchanged despite improvement of reciprocal movement in one patient, and was enhanced despite reduction in muscle strength in the other patient. The excitability of spinal inhibitory pathways at rest was not always reflected by motor function in spastic patients.

Facilitation of agonist motoneurons upon initiation of rapid and slow voluntary movements in man

The time course of facilitation of the agonist motoneurons upon initiation of voluntary ankle dorsiflexion was investigated in eight healthy subjects. The H-reflex and visually guided tracking methods were used for testing the excitability of the motoneuron pool and for controlling the initiation of movement as well as speed and force. Since the onset of voluntary EMG activity (EMG reaction time: EMGvRT) was delayed and/or obscured by test H-reflexes which were evoked very close to the behavioral responses, the subject was instructed to make response movements bilaterally, and EMGvRT was measured on the side without stimulation. In every subject, the EMGvRT was invariably longer in the ramp movement than in the step movement. The onset of H-reflex facilitation prior to EMG onset, which was regarded as indicating the arrival time of the descending motor command to the motoneuron pool, always started earlier in the ramp movement than in the step movement. The difference in facilitation onset between the two tasks was smaller than that in EMGvRT. Since the amplitude of the H-reflex at the onset of the voluntary EMG was equivalent in both movements, the development of H-reflex towards the behavioral EMG onset was more gradual in the ramp movement than in the step movement. The present results demonstrate that the longer reaction time in the slow ramp task depends on 2 factors: delay in the arrival of descending facilitatory impulses to the agonist motoneuron pool, and its slow recruitment thereafter.

Inhibition from the plantar nerve to soleus muscle during the stance phase of walking

The purpose of this study is to investigate the effect and the circuit from the branch of tibial (plantar) nerve to soleus muscle and its modulation during walking in humans. Stimulation of the plantar nerve produced short latency inhibition of soleus EMG activity and the H-reflex in humans. The threshold of afferent fibers was lower than that of motor fibers. This inhibition did not converge to disynaptic reciprocal Ia inhibition nor did inhibition from the cutaneous nerve of the big toe, but to Ib inhibition from the medial gastrocnemius nerve. The inhibitory pathway from the plantar nerve therefore is considered to include Ib inhibitory interneurones. Modulation of the inhibition was investigated during walking. Less EMG depression after plantar nerve stimulation occurred in the stance phase of walking than for tonic or dynamic plantar flexion at similar background EMG activity level. The inhibition of the soleus H-reflex after plantar nerve stimulation was also decreased during the stance phase. For investigating the influence of load on the inhibition from the plantar nerve, more EMG depression occurred in the stance phase with body unloading. Similar findings were observed in Ib inhibition from the medial gastrocnemius nerve, but not in disynaptic reciprocal Ia inhibition to soleus muscle. It is concluded that transmission of inhibition from the plantar nerve to soleus muscle is modulated during walking. It would minimize this inhibition during the stance phase of walking and might enhance soleus muscle activity via this reflex pathway for the support of weight.

Reassessment of H‐reflex recovery curve using the double stimulation procedure

We conducted two types of experiments to assess the validity of the H‐reflex recovery test, using double stimulation to test soleus motoneuron pool excitability in healthy and spastic subjects. One type dealt with the mechanical effect of the conditioning H reflex on the ankle joint; the other type with the effect of change in reflex size. The mechanical effect was tested both with the ankle joint fixed (FX) and free to move (FR). Differences between FX and FR conditions commenced with relaxation of soleus muscle contraction by the conditioning H reflex. In the FR condition, abrupt facilitation occurred, and changed to marked depression. We conclude that specific facilitation and inhibition in the FR condition were secondary effects of group Ia inflows caused by the ankle extensor muscle stretching on relaxation. In some spastic patients as well as in controls, facilitation due to the mechanical effect in the FR condition was observed despite the FX condition. The effects of systematic changes on soleus H‐reflex size were investigated at conditioning–test intervals of 80 ms, so as to avoid mechanical effects. When conditioning and test reflexes were the same size, the amount of recovery increased as the H‐reflex size increased. Comparison of the relation between amount of recovery and H‐reflex size, expressed as a percentage of Mmax, showed no significant difference between the two groups. We speculate that the stronger recovery of spasticity mentioned in previous literature may have resulted from the fact that relatively greater H reflexes were tested in those studies. In conclusion, the present study indicates that double stimulation is not appropriate for assessing spinal motoneuron pool “excitability increase” in spasticity.

Discharge of muscle afferents during voluntary co-contraction of antagonistic ankle muscles in man

The discharge of 38 tibialis anterior (TA) muscle spindle endings was recorded at rest and during isometric voluntary contraction of the ankle joint in eight healthy human subjects. With the ankle joint in 110 degrees plantarflexion, 24 endings (61%) were tonically active in the resting subject. During weak voluntary dorsiflexion, seven additional endings were activated, so that a total of 31 endings were active (82%). 24 of these were either newly recruited or discharged at a faster rate than at rest (average discharge rate 6.6 Hz at rest, 9.7 Hz during contraction). At matched levels of TA EMG, one ending was newly recruited and 10 were more active during co-contraction of dorsi and plantar flexors than during isolated dorsiflexion. 26 endings were equally active during the two tasks and one ending decreased its firing rate with co-contraction. Four of the 11 endings, which had a higher discharge rate during co-contraction than during dorsiflexion, discharged faster during plantarflexion than at rest although slower than during co-contraction. Plantarflexion had no effect on the discharge of three endings. The remaining four endings were not investigated during plantarflexion. It is suggested that the increased discharge rate of muscle endings during co-contraction is caused either by small changes in the length of the TA muscle or by a disproportionately high fusimotor drive during co-contraction.

Quantitative evaluation of movement disorders in neurological diseases based on EMG signals

In this paper, we propose a new method to make a quantitative evaluation for movement disorders. Based on the EMG signals, we analyzed the movement disorders for cerebellar patients at the motor command level. As an experimental task, we asked subjects to perform step-tracking wrist movements with a manipulandum, and simultaneously recorded wrist joint movements and muscle activities of four wrist prime movers with surface electrodes. In order to quantitatively evaluate the correspondence between the movement kinematics and the activities of the four muscles, we approximated the relationship between the wrist joint torque calculated from the kinematics and the four EMG signals using a dynamics model of wrist joint. Our surprising observation was that there was very high correlation between the wrist joint torque and the EMG signals. In fact, we identified causal abnormality of muscle activities for movement disorders of cerebellar patients, confirming effectiveness of our proposed method for analysis of movement disorders at the level of the motor command.

The Functional Role of the Cerebellum in Visually Guided Tracking Movement

We propose a new method to provide a functional interpretation of motor commands (i.e., muscle activities) and their relationship to movement kinematics. We evaluated our method by analyzing the motor commands of normal controls and patients with cerebellar disorders for visually guided tracking movement of the wrist joint. Six control subjects and six patients with cerebellar disorders participated in this study. We asked the subjects to perform visually guided smooth tracking movement of the wrist joint with a manipulandum, and recorded the movements of the wrist joint and activities of the four wrist prime movers with surface electrodes. We found a symmetric relationship between the second-order linear equation of motion for the wrist joint and the linear sum of activities of the four wrist prime movers. The symmetric relationship determined a set of parameters to characterize the muscle activities and their similarity to the components of movement kinematics of the wrist joint. We found that muscle activities of the normal controls encoded both the velocity and the position of the moving target, resulting in precise tracking of the target. In contrast, muscle activities of the cerebellar patients were characterized by a severer impairment for velocity control and more dependence on position control, resulting in poor tracking of the smoothly moving target with many step-like awkward movements. Our results suggest that the cerebellum plays an important role in the generation of motor commands for smooth velocity and position control.

A New Method for Functional Evaluation of Motor Commands in Patients with Cerebellar Ataxia

Quantitative evaluation of motor functions of patients with cerebellar ataxia is vital for evidence-based treatments and has been a focus in previous investigations of movement kinematics. Due to redundancy of the musculoskeletal system, muscle activities contain more information than the movement kinematics. Therefore, it is preferable to analyze causal anomalies of muscle activities to evaluate motor functions in patients. Here we propose a new method to evaluate the motor functions at the level of muscle activities and movement kinematics. Nineteen patients and 10 control subjects performed two movement tasks of the wrist joint, a step-tracking task and a pursuit task, with a manipulandum. The movements of the wrist joint and activities of the four wrist prime movers were recorded. We developed a linear model for the wrist joint to approximate the causal relationship between muscle activities and movement kinematics in terms of the wrist joint torque. We used a canonical correlation analysis to verify the causality between the muscle activities and the movement kinematics in the model. We found that the activities of the four muscles were related almost entirely to the position and velocity, with negligible correlation with the acceleration of the wrist joint. Moreover, the ratio of the weights for position- and velocity-related torque components characterized the contents of the muscle activities in terms of the movement kinematics. Next, we compared the ratios for the two movement tasks between the controls and patients. In control subjects, the ratios indicated clear task-specific changes that conformed to the functional requirements of the tasks. In contrast, in patients, the task-specific changes diminished highly significantly. The present results indicate that this ability to accommodate motor commands to the task requirements provides a novel quantitative parameter to characterize motor functions in patients with cerebellar ataxia.