Presynaptic Modulation of Ia Afferents in Young and Old Adults When Performing Force and Position Control

Abstract

Baudry S, Maerz AH, Enoka RM. Presynaptic modulation of Ia afferents in young and old adults when performing force and position control. J Neurophysiol 103: 623-631, 2010. First published November 25, 2009 doi:10.1152/jn.00839.2009. The present work investigated presynaptic modulation of Ia afferents in the extensor carpi radialis (ECR) when young and old adults exerted a wrist extension force either to support an inertial load (position control) or to achieve an equivalent constant torque against a rigid restraint (force control) at 5, 10, and 15% of the maximal force. H reflexes were evoked in the ECR by stimulating the radial nerve above the elbow. A conditioning stimulus was applied to the median nerve above the elbow to assess presynaptic inhibition of homonymous Ia afferents (D1 inhibition) or at the wrist (palmar branch) to assess the ongoing presynaptic inhibition of heteronymous Ia afferents that converge onto the ECR motor neuron pool (heteronymous Ia facilitation). The young adults had less D1 inhibition and greater heteronymous Ia facilitation during the position task (79 and 132.1%, respectively) compared with the force task (69.1 and 115.1%, respectively, P Ͻ 0.05). In contrast, the old adults exhibited no difference between the two tasks for either D1 inhibition (ϳ72%) or heteronymous Ia facilitation (ϳ114%). Contraction intensity did not influence the amount of D1 inhibition or heteronymous Ia facilitation for either group of subjects. The amount of antagonist coactivation was similar between tasks for young adults, whereas it was greater in the position task for old adults (P ϭ 0.02). These data indicate that in contrast to young adults, old adults did not modulate presynaptic inhibition of Ia afferents when controlling the position of a compliant load but rather increased coactivation of the antagonist muscle.

The optimal neural strategy for a stable motor task requires a compromise between level of muscle cocontraction and synaptic gain of afferent feedback

“…Therefore, the impact of the afferent feedback on the agonist and antagonist motor neuron populations is reduced, although it is possible that an increased gamma drive may increase spindle output and thereby in part compensate for the decreased synaptic gain (Llewellyn et al 1990;. Baudry et al (2010) showed that young subjects increased the afferent gain when exposed to a more unstable task, whereas older subjects, who are less able to modulate presynaptic inhibition (Butchart et al 1993;Koceja and Mynark 2000), reacted with an increase in the cocontraction level. These observations suggest that cocontraction can be considered a more easily applied strategy that is often the first choice when a subject is exposed to an unknown environment, whereas it is more difficult, but also more desirable because of metabolic costs, to adjust the afferent gains to the appropriate level.…”

“…Simultaneous activation of antagonist muscles, however, not only is a strategy used to achieve stability but is also necessary to perform certain movements. For example, the extensor and flexor carpi radialis are antagonists with respect to wrist flexion/extension but act as synergistic muscles during radial deviation of the wrist (Baudry and Enoka 2009). This implies that the cocontraction of antagonist muscles and stretch-sensitive afferent feedback should not be considered only as alternative strategies to achieve stability, as they often need to coexist and be tuned to reach the optimal compromise for output steadiness.…”

“…This is often termed reflex task dependence. For example, reflex amplitudes are higher during dynamic movement compared with matched isometric contractions (Baudry et al 2010;Baudry and Enoka 2009;Bawa and Sinkjaer 1999), and the afferent gain was observed to increase in parallel with the instability of a dynamic task (Pinar et al 2010). In this study, we hypothesized that these task-dependent changes in the magnitude of the afferent input to motor neurons reflect a deliberate strategy of the CNS: when a task is performed in an unstable environment, the afferent gain is high to minimize the impact of external perturbations at the expense of the risk of motor system resonance.…”

Motor unit activity when young and old adults perform steady contractions while supporting an inertial load

“…Because aging is associated with declines in sensory sensitivity, slowing of conduction velocity, and reductions in the amplitude of the responses evoked in spinal pathways (Burke and Kamen 1996;Chung et al 2005;Corden and Lippold 1996;Kido et al 2004;Nadler et al 2002;Tang and Woollacott 1999), old adults modulate afferent feedback less than young adults when performing voluntary actions and tend to rely more on adjusting levels of agonist and antagonist coactivation (Baudry et al 2010). For example, old adults limit the gain of responses arising from the muscle spindle relative to young adults in response to changes in posture and accompanying muscle contractions (Angulo-Kinzler et al 1998;Tsuruike et al 2003) by modulating presynaptic inhibition of Ia afferents less when proceeding from rest to a submaximal contraction (Butchart et al 1993;Earles et al 2001;Morita et al 1995) and when changing from a supine to a standing posture (Koceja and Mynark 2000), and they use less reciprocal Ia inhibition during movement (Hortobágyi et al 2006;Kido et al 2004).…”

“…To provide insight on age-associated adaptations in the integration of synaptic input by motoneurons, the approach focused on the discharge characteristics of the motor units when they were recruited during sustained con-tractions with different inertial loads. Because of the greater reliance by old adults on agonist-antagonist coactivation rather than modulation of spinal reflex pathways when confronted with a change in load compliance (Baudry et al 2010), the hypothesis was that old adults would exhibit less modulation of motor unit discharge across the two inertial loads than young adults.…”