Changes in corticospinal excitability during the preparation phase of ballistic and ramp contractions

Abstract

Key points Changes in corticospinal excitability prior to a contraction may depend on its characteristics, including the rate of torque development. This study compared the specific modulation of cortical and spinal excitability during the preparation phase (last 500 ms before contraction) of fast (ballistic) and ramp contractions of ankle dorsiflexors, using transcranial magnetic stimulation and peripheral nerve stimulation. The results indicate earlier changes at the cortical than at the spinal level during the preparation phase of both contraction types. However, these adjustments are delayed prior to ballistic relative to ramp contractions. This study suggests that the time course of change in cortical and spinal excitability during the preparation phase of a voluntary action is specific to the intended rate of torque development of the upcoming contraction. Abstract The present study investigated cortical and spinal excitability during the preparation phase of ballistic (BAL) and ramp (RAMP) isometric contractions. To this end, young adults performed BAL and RAMP (1500 ms torque rise time) contractions, reaching a similar torque level, with the ankle dorsiflexor muscles. Transcranial magnetic stimulation of the motor cortex was randomly applied to record motor evoked potentials (MEP) in the tibialis anterior during the last 500 ms preceding the contraction (n = 16). Short‐interval intracortical inhibition (SICI; n = 10) and spinal motor neurone excitability (F‐wave occurrence; n = 8) were also assessed during this period. Data were averaged over 100 ms time windows beginning 500 ms prior to the onset of contractions. An increase in MEP amplitude and a decrease in SICI were observed from the 200–100 ms and 300–200 ms time windows prior to BAL and RAMP contractions (P < 0.05), respectively, with greater changes prior to RAMP than to BAL within the 300–200 ms time window (P < 0.05). F‐wave occurrence, used to assess spinal motor neurone excitability, increased prior to RAMP (200–100 ms, P < 0.05) but not BAL contractions. Data obtained in a few participants during the last 100 ms confirmed a delayed and steeper rise in corticospinal excitability prior to BAL contractions. These results indicate earlier changes at the cortical than at the spinal level, with delayed changes prior to BAL contractions. This study suggests that the time course of change in cortical and spinal excitability during the preparation phase of a voluntary action is specific to the intended rate of torque development of the upcoming contraction.

Proactive inhibition is marked by differences in the pattern of motor cortex activity during movement preparation and execution

“…The ability to shift the distribution of CSE between neuronal inputs may allow for qualitatively equivalent movements to be performed in a variety of ways depending on task-specific goals ( 36 ). In fact, a recent study by Baudry and Duchateau ( 37 ) has shown that CSE rise time before EMG onset occurs 100 ms earlier for smooth ramp than ballistic contractions of tibialis anterior (akin to the response-locked analysis in the present study). They proposed that the difference in rise time was related to differences in how short-interval intracortical inhibition (SICI) changed before EMG onset: a sharp decrease in SICI was observed 200–100 ms before EMG onset for ballistic contractions, whereas SICI decreased smoothly over time for ramp contractions ( 37 ).…”

“…In fact, a recent study by Baudry and Duchateau ( 37 ) has shown that CSE rise time before EMG onset occurs 100 ms earlier for smooth ramp than ballistic contractions of tibialis anterior (akin to the response-locked analysis in the present study). They proposed that the difference in rise time was related to differences in how short-interval intracortical inhibition (SICI) changed before EMG onset: a sharp decrease in SICI was observed 200–100 ms before EMG onset for ballistic contractions, whereas SICI decreased smoothly over time for ramp contractions ( 37 ). This suggests that intracortical dynamics can be flexibly adapted depending on how the movement is made.…”

Probing the Link Between Cortical Inhibitory and Excitatory Processes and Muscle Fascicle Dynamics

“…This nding is well in line with the differential characteristics of GABA-A and GABA-B receptors as SICI was shown to be mainly driven by fast-acting GABA-A receptor types 9,21,22 while LICI is associated with slower-acting GABA-B receptors 23,24 . In support of this, it was shown that SICI can be modulated within 100ms during the preparation phase of ballistic dorsi exions 25 . In needs to be mentioned though, that one study showed potential spinal contributions to LICI in a very limited number of subjects 26 and we therefore cannot entirely rule out spinal in uences to the modulations in LICI shown in Fig.…”

Reticulospinal drive increases maximal motoneuron output in humans

“…Nevertheless, the contribution of cortical influences to startling stimuli cannot be fully excluded (Marinovic and Tresilian, 2016), and similarly, the performance of a rapid, high-force task likely has a cortical component. For example, Baudry and Duchateau (2021) observed a specific response in the preparatory phase of rapid, compared to slower ramp contractions, including a steeper and delayed rise in corticospinal excitability, intracortical disinhibition, with only a limited increase in spinal excitability, suggesting a role of the primary motor cortex in encoding rapid contractions. It should be noted, however, that our results do not necessary conflict with those of Baudry and Duchateau (2021), but rather complement them.…”

“…For example, Baudry and Duchateau (2021) observed a specific response in the preparatory phase of rapid, compared to slower ramp contractions, including a steeper and delayed rise in corticospinal excitability, intracortical disinhibition, with only a limited increase in spinal excitability, suggesting a role of the primary motor cortex in encoding rapid contractions. It should be noted, however, that our results do not necessary conflict with those of Baudry and Duchateau (2021), but rather complement them. Indeed, there is an extensive network of cortico-reticular connections (Fregosi et al, 2017; Darling et al, 2018; Fisher et al, 2021; Figure 1C), thus in response to a startling stimulus, cortical inputs will likely be amplified by the reticulospinal neurons leading to a greater motoneuron output.…”