Rapid Motor Responses Are Appropriately Tuned to the Metrics of a Visuospatial Task

Abstract

Considerable research has established that rapid motor responses (traditionally called reflexes), can be modified by a subject's voluntary goals. Here, we expand on past observations using verbal instructions by defining the voluntary goal via visual target position. This approach allowed us to objectively enforce task adherence and explore a richer set of variables, such as target direction and distance, metrics that modify voluntary control and that--according to our hypothesis--will influence rapid motor responses. Our first experiment tested whether upper-limb responses are categorically modulated by target direction by placing targets such that the same perturbation could push the hand into one target and out of the other, a spatial analogue to "resist/yield" verbal instructions. Consistent with these classical results, we found that the short-latency rapid response (R1, 20-45 ms) was not modulated by target direction, whereas long-latency rapid responses (R2/R3, 45-105 ms) were modified in a manner approaching the voluntary response (VOL, 120-180 ms). Our second experiment tested whether upper-limb responses are continuously modulated by target distance by distributing five targets along one axis centered on the hand. Here, the long-latency and voluntary response mirrored the task demands by increasing activity in a graded fashion with increasing target distance. Our final experiment explored how upper-limb responses incorporate two-dimensional spatial information by placing targets radially around the hand. Notably, long-latency responses exhibited smooth tuning functions to target direction that were similar to those observed for the voluntary response. Taken together, these results illustrate the flexibility of long-latency rapid responses and emphasize their similarity to later voluntary responses.

Goal-dependent modulation of the long-latency stretch response at the shoulder, elbow, and wrist

“…He found that, although the verbal instruction did not modulate the short-latency stretch response (i.e., 25-50 ms postperturbation onset), the magnitude of the long-latency stretch response was larger when participants were instructed to resist the perturbation. Since this seminal work, similar patterns of goal-dependent modulation have been shown in many muscles, including those acting at the jaw (Johansson et al 2014), shoulder (Kurtzer et al 2014;Nashed et al 2012;Omrani et al 2013;Pruszynski et al 2008), elbow (Cluff and Scott 2013;Colebatch et al 1979;Crago et al 1976;Evarts and Granit 1976;Nashed et al 2012Nashed et al , 2014Omrani et al 2013;Pruszynski et al 2008Pruszynski et al , 2011bRavichandran et al 2013;Rothwell et al 1980;Shemmell et al 2009), wrist (Calancie andBawa 1985;Jaeger et al 1982; Lee and Tatton 1982;Manning et al 2012), finger (Capaday and Stein 1987;Cole et al 1984;Marsden et al 1981), and ankle (Gottlieb and Agarwal 1979;Ludvig et al 2007). …”

“…If the participant's response was inaccurate (i.e., missed the target) or too slow (i.e., took longer than 375 ms to reach the target), the target color would change from white to red to indicate an error-otherwise, the target color would change from white to green ( Fig. 1D; see also Pruszynski et al 2008). Participants completed 20 trials of each of the 24 experimental conditions (3 joint segments: shoulder, elbow, wrist; 2 preloads: flexion, extension; 2 perturbation loads: flexion, extension; 2 targets: left, right) in a randomized order totaling 480 trials.…”

Fast corrective responses are evoked by perturbations approaching the natural variability of posture and movement tasks

“…We followed classic definitions of the different epochs of time found in the literature (Crago et al 1976;Lee and Tatton 1982;Nakazawa et al 1997;Pruszynski et al 2008). The first epoch (R1) occurs from 20 to 45 ms postperturbation and is referred to as the short-latency response.…”

“…The overlap in distribution between perturbation-induced motion and the natural variability was addressed by receiver operating characteristic (ROC) analysis (Corneil et al 2004;Pruszynski et al 2008). This technique is used to compute a time series of estimates of the probability to discriminate two random variables based on their empirical distribution.…”

“…For example, spinal reflexes of the arm can counter mechanical perturbations in as little as 20 -40 ms. These purely spinal processes are followed by long-latency responses (50 -105 ms) that can be modulated by explicit task goals (Crago et al 1976;Marsden et al 1981;Mutha et al 2008;Pruszynski et al 2008;Rothwell et al 1980) and use internal models of limb and environmental dynamics (Gielen et al 1988;Kimura and Gomi 2009;Krutky et al 2010;Kurtzer et al 2008Kurtzer et al , 2009Soechting and Lacquaniti 1988). In this respect, the capabilities of longlatency responses mirror those shown in voluntary control.…”