It has been argued that modulation of the H-reflex during dynamic activities reflects changes in motoneurone excitability brought about to suit the functional demands of the task. Reflex modulation has been reported during various dynamic tasks including passive single joint movements (Mark et al. 1968; Gottlieb & Agarwal, 1978; Robinson et al. 1982; Etnyre & Abraham, 1986; Romano & Schieppati, 1987; Guissard et al. 1988; Voigt & Sinkjaer, 1998) and multijoint movements such as stepping and cycling (Brooke et al. 1995a; Cheng et al. 1995a; Misiaszek et al. 1995a), as well as during more functional tasks such as walking and running (Capaday & Stein, 1986, 1987a; Yang & Whelan, 1993; Faist et al. 1996; Simonsen & Dyhre-Poulsen, 1999). Factors that are known to alter H-reflex amplitude include the level of background activation (Butler et al. 1993), muscle length (Gerilovsky et al. 1989), movement velocity (Romano & Schieppati, 1987), activation history (Proske et al. 1993; Gregory et al. 1998) and muscle composition (Messina & Cotrufo, 1976). Although a number of mechanisms have been proposed to account for H-reflex modulation, such as homosynaptic post-activation depression and presynaptic inhibition of Ia afferents, the origin and functional significance of such modulation is still unclear. Much of the debate concerning this issue may hinge around methodological differences and the generalization of findings between functionally different tasks.
It is generally agreed that the H-reflex is strongly modulated throughout the gait cycle (Capaday & Stein, 1986, 1987a; Yang & Whelan, 1993; Garrett et al. 1994; Faist et al. 1996; Simonsen & Dyhre-Poulsen, 1999). For example, Capaday & Stein (1986) reported an increase in soleus (SOL) H-reflex amplitude late in the stance phase when the triceps surae is active to propel the body forward and an absence during the swing phase when the foot is dorsiflexed and SOL activation would hinder movement. However, Yang & Whelan (1993) showed the SOL H-reflex to be depressed despite voluntary activation of the SOL during the swing phase, indicating that this reflex modulation was not merely a consequence of central drive, and suggested presynaptic inhibition of primary afferents as a likely mechanism. Moreover, Capaday & Stein (1987a) reported that when gait velocity increased from walking (4 km h−1) to running (8 km h−1), a decrease in SOL H-reflex amplitude occurred despite increased underlying SOL activation.
Functional reflex modulation has also been reported during landing and hopping tasks (Moritani et al. 1990; Dyhre-Poulsen et al. 1991). In the study of Dyhre-Poulsen et al. (1991) the SOL H-reflex was strongly inhibited when landing from a downward jump with the inhibition commencing up to 100 ms prior to foot contact. During hopping, however, the SOL H-reflex increased before foot contact despite a reduction in SOL EMG and in the presence of antagonist activation. The functional significance of this modulation was interpreted in relation to muscle stiffness and the transfer of muscle from a spring to a damping unit. Moritani et al. (1990) investigated reflex modulation in two functionally different muscles, SOL and medial gastrocnemius (MG), during hopping tasks of different heights and frequencies. H-reflexes were modulated differently in the two muscles with those in the ‘fast’ MG increasing as the amplitude and frequency of jumping movements increased whereas those in SOL decreased. These findings support the notion that these peripheral reflexes are modulated in a manner to suit the functional demands of the task. However, caution must be taken when interpreting the amplitude of the reflex response in a functional sense, as Kearney et al. (1999) have reported that the reflex EMG response does not necessarily correspond to the resultant reflex torque.
Regardless of the resultant torque contribution, the fact that modulation of reflex amplitude is somewhat independent of central drive indicates that reflex magnitude is not merely a reflection of motoneurone excitability, but can also be influenced by additional neural mechanisms. In the light of model-based simulations of reflex output from a motoneurone pool (Capaday & Stein, 1987b), and experimental evidence from decerebrate cats (Capaday & Stein, 1989), it is the prevailing view of the Capaday group that the observed reflex modulation during gait was due to a centrally regulated increase in the presynaptic inhibition of Ia terminals. It was postulated that the functional significance of such a mechanism was to reduce central gain of the stretch reflex to avoid saturation of the motor output during running.
While Brooke et al. (1995b) agree that the mechanism of this reflex depression is acting at a premotoneuronal level, they suggest a peripheral origin for this inhibitory influence. During passive stepping and cycling movements modulation of the SOL H-reflex corresponded to movements of the knee and hip joints and was attributed to the influence of heteronymous Ia afferents arising from the lengthening quadriceps muscles (Brooke et al. 1995a). However, the relevance of these findings to reflex modulation during human gait was recently challenged by Schneider et al. (2000) and Garrett et al. (1999), who found a limited influence of knee motion on SOL H-reflex modulation during human gait. Unfortunately, the inhibitory influence of motion about the hip was not controlled and therefore cannot be ruled out as a potential inhibitory mechanism.
Significant H-reflex depression has been recorded within 50 ms of the onset of passive pedalling, a latency that precludes the involvement of higher motor centres (Brooke et al. 1995b). Similar rapid reflex modulation has been reported in spinal cord-injured patients during passive pedalling (Brooke et al. 1995b) and passive, sinusoidal ankle rotations (Voigt & Sinkjaer, 1998), again suggesting a peripheral origin for this reflex modulation.
Although some authors attribute inhibition of the SOL H-reflex to heteronymous Ia afferent influences resulting from hip and knee movement (Brooke et al. 1995a; Misiaszek et al. 1995a), a long-lasting reflex depression may also arise from homonymous influences (Hultborn et al. 1996; Wood et al. 1996; Kohn et al. 1997). Hultborn et al. (1996) investigated long-lasting depression of the SOL H-reflex following passive triceps surae lengthening. From experiments on both humans and cats, it was shown that the reduction in H-reflex amplitude was related to depression of Ia transmission specific to the afferent fibres related to the dynamic task (homonymous Ia afferents). Furthermore, this inhibition was seen without alteration to motoneurone excitability and, although a dorsal root potential was recorded, indicating activity of presynaptic inhibitory interneurones, the time course of this potential (< 500 ms) was considerably shorter than the long-lasting inhibition of the H-reflex (8-12 s). The authors postulated that this phenomenon was due to the reduced probability of transmitter release from the Ia fibres (homosynaptic post-activation depression) rather than traditional GABAergic presynaptic inhibition.
Similar long-lasting H-reflex depression (up to 15 s) has been reported following passive triceps surae lengthening (Wood et al. 1996), during passive cycling movements (Misiaszek et al. 1995a) and following a quadriceps tendon tap (Cheng et al. 1995b). In the study of Wood et al. (1996) equivalent experiments were performed in the cat in which muscle spindle firing was assessed during the preceding muscle stretch. Modulation of H-reflex amplitude appeared to coincide with increased muscle spindle discharge associated with the preceding change in muscle length. However, in the experiments of Misiaszek et al. (1995a) and Cheng et al. (1995b) the ankle was braced to prevent changes in SOL muscle length and, hence, prevent variations in the discharge of homonymous Ia afferents. Therefore, long-lasting H-reflex depression may occur in the absence of homonymous Ia afferent influences (Cheng et al. 1995b; Misiaszek et al. 1995a) or without variations in the discharge of heteronymous Ia afferents (Hultborn et al. 1996; Wood et al. 1996). Based on these findings, one may speculate that: (1) different peripherally mediated inhibitory mechanisms are responsible for the long-lasting H-reflex depression seen during single passive joint rotation and multijoint movements, or (2) a single, centrally modulated inhibitory mechanism is responsible for the long-lasting reflex modulation seen during both single and multijoint movements.
In an attempt to better understand the mechanisms at play during single passive joint rotations this study was conducted with two primary objectives. Firstly, H-reflex modulation was examined during lengthening and shortening actions of the triceps surae under tightly controlled experimental procedures to ensure that alterations in reflex magnitude were not due to variations in effective stimulus intensity. Secondly, although short latency (< 50 ms) reflex modulation has been recorded during passive cycling movements, presumably due to heteronymous Ia influences, to our knowledge, reflex modulation has not been investigated over a similar short latency during passive single joint movements involving homonymous Ia afferents. Therefore, reflex responses were recorded at various latencies following the onset of movement in an attempt to determine the time-course of homonymous Ia afferent influences on H-reflex amplitude. Additionally, H-reflexes were recorded from both SOL and MG during all experiments to assess whether reflex modulation was influenced by the functional characteristics of a muscle.