Instruction-dependent modulation of the long-latency stretch reflex is associated with indicators of startle

Abstract

Long-latency responses elicited by postural perturbation are modulated by how a subject is instructed to respond to the perturbation, yet the neural pathways responsible for this modulation remain unclear. The goal of this study was to determine if instruction-dependent modulation is associated with activity in brainstem pathways contributing to startle. Our hypothesis was that elbow perturbations can evoked startle, indicated by activity in the sternocleidomastoid muscle (SCM). Perturbation responses were compared to those elicited by a loud acoustic stimulus, known to elicit startle. Postural perturbations and startling acoustic stimuli both evoked SCM activity, but only when a ballistic elbow extension movement was planned. Both stimuli triggered SCM activity with the same probability. When SCM activity was present, there was an associated early onset of triceps EMG, as required for the planned movement. This early EMG onset occurred at a time often attributed to long-latency stretch reflexes (75-100ms). The nature of the perturbation-triggered EMG (excitatory or inhibitory) was independent of the perturbation direction (flexion or extension) indicating that it was not a feedback response appropriate for returning the limb to its original position. The net EMG response to perturbations delivered after a movement had been planned could be explained as the sum of a stretch reflex opposing the perturbation and a startle-evoked response associated with the prepared movement. These results demonstrate that rapid perturbations can trigger early release of a planned ballistic movement, and that this release is associated with activity in the brainstem pathways contributing to startle reflexes.

Voluntary reaction time and long-latency reflex modulation

“…Recent work has shown that perturbations applied to the elbow (Ravichandran et al 2013) or ankle (Campbell et al 2013) can elicit a startle reflex, characterized by activation of sternoicleidomastoid (SCM). Important for the context of the present study, startling stimuli are known to involuntarily trigger prepared movements at short latencies (Ͻ100 ms), a phenomenon known as the StartReact effect (for reviews, see Carlsen et al 2012;Rothwell et al 2006;Shemmell et al 2015).…”

“…Finally, magnitude of the voluntary response was captured in an epoch (VOL) occurring between 100 and 200 ms postperturbation. Previous studies (e.g., Lee and Tatton 1978;Pruszynski et al 2008Pruszynski et al , 2009Ravichandran et al 2013) have used a similar temporal segregation to more closely analyze the timecourse of M2 as well as the voluntary response.…”

“…One view attributes the amplitude modulation to be the result of an increase in the excitability of the reflex pathways (Calancie and Bawa 1985;Colebatch et al 1979;Hammond 1956; Lee and Tatton 1978;Pruszynski et al 2008;Selen et al 2012;Yang et al 2011). The opposing view suggests that the amplitude modulation is an artifact of the superposition of the voluntary response onto the end of the long-latency response (Crago et al 1976;Houk 1978; Lewis et al 2006;Manning et al 2012;Ravichandran et al 2013;Rothwell et al 1980). Part of the disagreement appears to stem from the problem of clearly delineating the M2 response from the voluntary response in EMG recordings.…”

“…Although Hammond (1956) originally assumed that the M2 and voluntary responses did not overlap in time, there is evidence showing that voluntary RTs to a mechanical perturbation can be considerably shorter than 100 ms (e.g., Day et al 1983;Evarts and Granit 1976;Evarts and Vaughn 1978;Lewis et al 2006;MacKinnon et al 2000;Manning et al 2012;Ravichandran et al 2013;Shemmell 2009Shemmell , 2015. As an example, to dissociate M2 from voluntary activity, Evarts and Granit (1976) instructed participants to supinate or pronate the forearm in response to a perturbation (occurring either in the supination or pronation direction).…”

“…In contrast, when the same supination response was required in reacting to a supination perturbation, M1 and M2 appeared in pronators but only the voluntary response remained in biceps. Using this technique, Evarts and Granit (1976) and others (e.g., Evarts and Vaughn 1978;MacKinnon et al 2000;Ravichandran et al 2013) reported voluntary RTs to a proprioceptive stimulus to be as short as 70 ms. Assuming similar RTs when M2 and the voluntary response occurred in the same muscle, any observed M2 modulation could have resulted from overlapping voluntary activity onto the M2 response.…”