Department of Exercise Sciences


Uncoupling response inhibition

Hayley J. MacDonald, Cathy M. Stinear, and Winston D. Byblow
Published in J Neurophysiol 108: 1492-1500, 2012

Introduction

  • Response inhibition requires prevention of unwanted movement and is fundamental to human behaviour. It is challenging because it requires higher order control and is often impaired in neurodegenerative conditions.
  • When healthy adults must prevent a subset of prepared actions, execution of the remaining response is markedly delayed. Previously, Coxon and colleagues speculated that this delay was the result of rapid nonselective suppression of all prepared movements and subsequent selective reinitiation of the required movement.
  • An alternative way to conceptualize the process of selective movement prevention is the suppression of a single unitary response, which comprises all prepared movement components “coupled” together. All movements are coupled together into one response that now consists of multiple subcomponents. Movement prevention would therefore affect all subcomponents of the single response simultaneously. The response would then need to be separated into its subcomponents before selective reinitiation of only the required component could occur.
  • This separation would be achieved through uncoupling all the response components. If our model is correct, the uncoupling and reinitiation processes should be sensitive (under time pressure) to the strength of coupling between subcomponents in the prepared movement, which can be investigated using a bimanual task.

 

Aim

First, to further investigate the reselection and reinitiation processes presumed to occur during selective movement prevention tasks; and second, to investigate whether the delay in responding that occurs on selective trials depends on the degree of coupling between independent components of the previously prepared movement.

 

Method

  • Participants: fifteen healthy right-handed adults with no neurological impairment.
  • Behavioural task:
    • The bimanual anticipatory response inhibition (ARI) task was performed to exam selective response inhibition, by measuring the response times (and asynchrony between digits) during action execution and stopping performance. Electromyography was recorded from EIP (index finger extension) and APB (thumb abduction).
    • There were three types of Stop trials: Stop Both, when both indicators stopped automatically and Stop Left and Stop Right (selective trials), when only the left or right indicator stopped, respectively. Feedback also indicated whether inhibition of one or both responses was successful (Figure 1).
    • Each participant completed the task four times in different digit-pairing combinations, with the pairing combinations counterbalanced across participants. Each pairing required either bilateral index finger extension or thumb abduction (homogeneous pairings, i.e., strongly coupled), or a combination of the two (heterogeneous pairings, i.e., weakly coupled).
MacDonald-2012-Figure-1

 

Results

  • As expected, selective trials produced a delay in the remaining movement compared with execution trails. Successful performance in the selective condition occurred via suppression of the entire prepared response and subsequent selective reinitiation of motor output was sensitive to the degree of similarity between responses, occurring later but as a faster rate with homogeneous digits (Figure 4).
  • There were persistent aftereffects from the selective condition on the motor system, which indicated greater levels of inhibition and a higher gain were necessary to successfully perform selective trails with homogeneous pairings.
MacDonald-2012-Figure-4

 

Interpretation

 

Overall, the results support a model of inhibition of a unitary response and selective reinitiation, rather than selective inhibition.

 

This study has demonstrated that selective movement prevention occurs through rapid suppression of the prepared movement and subsequent reinitiation of the desired component of the response. This process results in a movement delay and is more difficult to achieve when the prepared response comprises strongly coupled components. The rapid suppression of the prepared response was not affected by the strength of coupling between digits. However, the reinitiation of the desired movement component was delayed and occurred at a higher rate when the prepared response involved same pairings of digits. This is the first study to show that a higher gain and possibly greater levels of inhibition are necessary to successfully perform selective reinitiation in strongly coupled postures. The carryover effects observed in the lift times of the left hand with homogeneous pairings further support this idea. Further research is needed to elucidate the neurophysiological mechanisms underlying the observed effects.

 

 

Acknowledgements

We thank Phil Lacey, Terry Corin, Mike Claffey, and Ryan McCardle for technical assistance. H. MacDonald is supported by a W.B.Miller PhD scholarship from the Neurological Foundation of New Zealand.