**2.2 Responses to passive shortening – Shortening reaction**

Besides abnormal muscle responses to stretch, anomalous reactions in the shortened muscles during a passive joint motion have also been described in Parkinson's disease. More than a century ago, Westphal (1877, 1880) observed muscular contraction in the passively shortened skeletal muscles. Before he observed this phenomenon, he had already studied the muscular contraction in lengthening or stretched muscles. Thus, he named it 'paradoxer Muskel-contraction'. At that time, he also described enhanced activation of tibialis anterior corresponding to the shortening phase in patients who had great difficulty in passively aiding imposed movement. The phenomenon he observed is often referred to as "Westphal's phenomenon". Later, Sherrington (1909) described analogous findings in both the spinal dog and the decerebrate cat under the name "shortening reaction'. This term has been used since then.

Application of electromyographic (EMG) recording method has demonstrated that inappropriate activation of shortened muscles occurs widely in basal ganglia disorders (Rondot & Metral, 1973), and most prominently in Parkinson's disease (Andrews et al., 1972; Angel, 1983; Berardelli & Hallett, 1984; Rondot & Metral, 1973; Xia & Rymer, 2004). An example of shortening reaction is illustrated in Fig. 1B (Xia et al., 2011). During the passive wrist flexion movement, flexor muscles were progressively shortened. There occurred strong muscle activations in the wrist flexor muscles. Shortening reaction has been reported to be manifested in both upper and lower limb muscles. Some investigators suggested that shortening reaction plays an important role in the pathophysiology of rigidity (Angel, 1983; Rondot & Metral, 1973), given that it represents a reflex action that agonistically assists with a passive movement in contrast to antagonistic opposition of a motion caused by stretch reflex. Correlational analysis showed that there was no direct relationship between shortening reaction and changes in muscle tone (Berardelli & Hallett, 1984).

Nevertheless, the neural mechanism of the shortening reaction was virtually unknown. Since shortening reaction was first reported a century ago, very little attention has been paid to exploring its underlying physiology. Shortening reaction is the opposite of stretch reflex, a topic that has been extensively studied for a long period of time. In contrast, only a limited number of studies were conducted to understand and characterize shortening reaction, and these previous studies simply monitored muscle electromyographic activity (Andrews et al. 1972; Angel, 1983; Berardelli et al. 1983; Berardelli and Hallett, 1984; Rondot and Metral, 1973). The importance of shortening reaction in the pathophysiology of parkinsonian rigidity is undoubtedly underestimated. Utilization of both EMG recording and joint torque measure has provided us with useful information to reveal the role of shortening reaction in mediating rigidity in Parkinson's disease (Xia & Rymer, 2004; Xia et al., 2011). A parallel mechanism responsible for mediating parkinsonian rigidity is stretch-induced inhibition which will be discussed in the next section.

Physiological and Biomechanical Analyses of Rigidity in Parkinson's Disease 489

In addition to shortening reaction, Sherrington (1909) also observed in the above-noted animal preparations that "*… when an examiner bent the knee against the knee-extensor's contraction, the examiner felt the opposition offered by the extensor gave away almost abruptly at a certain pressure; the knee could then be flexed without opposition ...*". He named this phenomenon "lengthening reaction". Lengthening reaction was demonstrated in both spinal dog and in decerebrate rigidity of the cat, yet the reaction was recognized to have differential features in the two preparations. In his monograph, he also pointed out that muscles, exhibiting shortening reaction and lengthening reaction, were all extensor muscles. The distinction of the flexor and extensor muscle groups has been documented in parkinsonian rigidity (Mera

The well-know clasp-knife phenomenon associated with human spasticity, appears to be the equivalent of the lengthening reaction (Burke et al., 1970, 1971). The clasp-knife reflex is characterized by an abrupt decline in muscle force that occurs when a spastic limb is moved beyond a certain joint angle. There is a common ground between lengthening reaction in animal preparations (Burke et al., 1972b; Rymer et al., 1979) and clasp-knife reflex in human spasticity in that the essential feature of both phenomena is the sudden release of the resistance due to continuous stretch of the elongated muscle, hence also referred to as "stretch-induced inhibition" (Rymer et al., 1979). The physiological framework previously established or explored in the context of the lengthening reaction or stretch-induced inhibition has recently been investigated in parkinsonian rigidity (Xia & Rymer, 2004; Xia et

Fig. 1C illustrates a stretch-induced inhibition recorded from a parkinsonian patient in the Off-medication state. During the passive flexion movement (Fig. 1A), there was a large initial stretch reflex in the wrist extensor muscles. The initial stretch reflex was followed by a period of sustained activity and curtailed by an evident decline when the progressive movement approached at almost the neutral position and the muscle length of the extensors was elongated, demonstrating the stretch-induced inhibition (Fig. 1C). It is noted that both shortening reaction and stretch-induced inhibition occur during the same movement phase (Fig. 1). The importance and functional role stretch-induced inhibition and the above described shortening reaction may have played in parkinsonian rigidity will be explained

This session will begin with an overview of the basic principles of muscle mechanics. When an active muscle is stretched, the muscle force output increases proportionally with the increasing muscle length. The dependence of muscle force on muscle length gives rise to a "spring-like" behavior (Gordon et al., 1966; Matthews, 1959; Rack & Westbury, 1969). This spring-like property of skeletal muscle has been shown to play a key role in the maintenance of posture and control of movement. A limb's posture is maintained when the forces exerted

Rotational movements about human joints are promoted by a resultant torque which is a summation of the individual contributions of agonist muscles minus contributions of antagonist muscles, where a single torque is mathematically defined as the product of force times the moment arm for each muscle. The corresponding measure of rotational position is the joint angle, which determines the length of each muscle acting on the joint. Ultimately, it

**3. Pathophysiological mechanisms of lead-pipe rigidity** 

by agonist and antagonist muscle groups are equal and opposite.

**2.3 Lengthening reaction or stretch-induced inhibition** 

et al., 2009; Xia et al., 2006).

and discussed in Section 3.

al., 2011).

Fig. 1. Kinematic and EMG recordings during passive flexion movement obtained from a patient after an overnight withdrawal of medication (Off-medication). **A.** Wrist joint position during the passive flexion movement; the subject's wrist joint was externally rotated from 30 degree to -30 degree at 50°/s. **B.** Shortening reaction was recorded in shortened flexors in the Off-medication state in a parkinsonian subject. There was an increased EMG activation in passively shortened muscles. **C.** Stretch-induced inhibition was observed in the stretched extensor muscles during the same movement. There was an EMG reduction, when the stretch exceeded the neutral position and the muscle length was elongated [from Xia et al. (2011) with permission].
