Age and Muscle-Dependent Variations in Corticospinal Excitability during Standing Tasks

<div><p>In this study, we investigated how modulation in corticospinal excitability elicited in the context of standing tasks varies as a function of age and between muscles. Changes in motor evoked potentials (MEPs) recorded in <i>tibialis anterior</i> (TA) and <i>gastrocnemius lateralis</i> (GL) were monitored while participants (young, n = 10; seniors, n = 11) either quietly stood (QS) or performed a heel raise (HR) task. In the later condition, transcranial magnetic stimulation (TMS) pulses were delivered at three specific time points during the task: 1) 250 ms before the “go” cue (preparatory (PREP) phase), 2) 100 ms before the heel rise (anticipatory postural adjustment (APA) phase), and 3) 200 ms after heel rise (execution (EXEC) phase). In each task and each phase, variations in MEP characteristics were analysed for age and muscle-dependent effects. Variations in silent period (SP) duration were also examined for certain phases (APA and EXEC). Our analysis revealed no major difference during QS, as participants exhibited very similar patterns of modulation in both TA and GL, irrespective of their age group. During the HR task, young adults exhibited a differential modulation in the PREP phase with enhanced responses in TA relative to GL, which was not seen in seniors. Finally, besides differences in MEP latency, age had little influence on MEP modulation during the APA and EXEC phases, where amplitude was largely a function of background muscle activity associated with each phase (i.e., APA: TA; EXEC: GL). No age or muscle effects were detected for SP measurements. Overall, our results revealed no major differences between young adults and healthy seniors in the ability to modulate corticospinal facilitation destined to ankle muscles during standing tasks, with maybe the exception of the ability to prime muscle synergies in the preparatory phase of action.</p></div

Mean MEP log-amplitude (upper panel) and latency (lower panel) computed in TA and GL in the two groups at each time delay/phase of the heel raising task.

<p>Symbols indicated significant main effects or interactions. Note that in the PREP phase, a significant group×muscle interaction (indicated by **, p<0.01) was found reflecting the difference in MEP amplitude between TA and GL. In the APA and EXEC phases, a significant main effect of muscle (indicated by ## and ###, p<0.01 and p<0.001 respectively) was found reflecting larger MEP amplitude in the TA and in the GL during their respective phase. A main effect of group (indicated by §, p<0.05) was found for MEP latency reflecting delayed latency in seniors in the APA and EXEC phases. Abbreviations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0110004#pone-0110004-g001" target="_blank">Figures 1</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0110004#pone-0110004-g002" target="_blank">2</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0110004#pone-0110004-g003" target="_blank">3</a>.</p

Examples of background electromyographic activity and of MEP recorded in TA and GL in a young and a senior participant during performance of the heel raise task.

<p>In each participant and for each muscle, the activity and MEP responses are given for each time delay (indicated by arrows) and their corresponding phase: PREP phase (1000 ms, 250 ms before the “go” cue); APA phase (100 ms before movement onset) and EXEC phase (200 ms after movement onset) respectively for the young and senior participants. The “go” cue is indicated by a speaker symbol. Abbreviations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0110004#pone-0110004-g001" target="_blank">Figures 1</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0110004#pone-0110004-g002" target="_blank">2</a>.</p

Characteristics of motor evoked potentials (MEP) recorded during quiet standing.

<p><b>A.</b> Examples of individual MEP traces recorded in TA and GL during quiet standing, in a young and a senior participant. <b>B.</b> Mean MEP log-amplitude and latency computed in each age group during quiet standing. Note that no main effect or interaction was detected. Abbreviations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0110004#pone-0110004-g001" target="_blank">Figure 1</a>.</p

Schematic representation of the experimental protocol and examples of muscle activity elicited in <i>tibialis anterior</i> (TA) <i>gastrocnemius lateralis (GL)</i> during performance of the heel raise (HR) task in participants of each age group.

<p>Responses to transcranial magnetic stimulation were recorded under two task conditions, quiet standing (QS, not shown here) and HR, with the latter task being subdivided in three phases. As shown in A, each HR trial (3000 ms epoch) included a warning signal (WS) in the form of an electrical pulse delivered at the dorsum of the foot at 250 ms (thin arrow symbol), followed by a “go” cue at 1250 ms in the form of an auditory tone lasting 1 s. Participants were instructed to synchronize the heel raising action with the tone. In the electromyographic traces shown in B, the onset of the anticipatory postural adjustment (APA) elicited in the TA in preparation for the upcoming action along with the actual onset of the heel raising action in the GL are clearly evident in the two participants, young and senior. Such recordings, obtained prior to TMS applications, were used to individually adjust stimulation delays during performance of the HR task. As illustrated in A (lightning symbol), the earlier time delay for TMS delivery was in the preparatory (PREP) phase at 1000 ms (i.e., 250 ms before the go cue), when participants prepare to the upcoming action. The second delay for TMS was set at 100 ms before movement onset in the APA phase, where participants moved their body forward to anticipate the heel raising action. Finally, TMS was delivered 200 ms after movement onset during actual execution of the heel raising action (EXEC).</p

Mean reaction time (± standard deviation) for dancers and non-dancers during quiet standing baseline trials and across the different dynamic postural conditions.

<p>Mean reaction time (± standard deviation) for dancers and non-dancers during quiet standing baseline trials and across the different dynamic postural conditions.</p

Dynamic postural control and associated attentional demands in contemporary dancers versus non-dancers

<div><p>Postural control is not a fully automatic process, but requires a certain level of attention, particularly as the difficulty of the postural task increases. This study aimed at testing whether experienced contemporary dancers, because of their specialized training involving the control of posture/balance, would present with a dual-task performance suggesting lesser attentional demands associated with dynamic postural control compared with non-dancers. Twenty dancers and 16 non-dancers performed a dynamic postural tracking task in both antero-posterior and side-to-side directions, while standing on a force platform. The postural task was performed, in turn, 1) as a stand-alone task, and concurrently with both 2) a simple reaction time task and 3) a choice reaction time task. Postural control performance was estimated through variables calculated from centre of pressure movements. Although no overall group difference was found in reaction time values, we found a better ability to control the side to side movements of the centre of pressure during the tracking task in dancers compared with non-dancers, which was dependent on the secondary task. This suggests that such increased ability is influenced by available attentional resources.</p></div

Reaction time.

<p>Percent change in reaction time from the quiet standing baseline condition for both the antero-posterior (AP) and side-to-side (ML) dynamic tracking tasks. Values for both the simple reaction time (SRT) and choice reaction time (CRT) secondary tasks are contrasted between dancers and non-dancers. Bars represent group mean plus standard error.</p

COP velocity.

<p>Centre of pressure (COP) velocity (cm/s) plotted for both the antero-posterior (AP) and side-to-side (ML) tasks. Results from dancers and non-dancers are contrasted. Data points represent group mean (with values from single task, SRT dual-task and CRT dual-task polled together) plus or minus standard error.</p

COP proximity.

<p>Centre of pressure (COP) proximity (cm) to the target plotted against the dual-task condition (single task, SRT dual-task, CRT dual-task) for both the antero-posterior (AP) and side-to-side (ML) tasks. Results from dancers (top panel) and non-dancers (bottom panel) are contrasted. Data points represent group mean plus or minus standard error.</p