N1-P2 event-related potentials and perceived intensity are associated: The effects of a weak pre-stimulus and attentional load on processing of a subsequent intense stimulus.

A weak stimulus presented immediately before a more intense one reduces both the N1-P2 cortical response and the perceived intensity of the intense stimulus. The former effect is referred to as cortical prepulse inhibition (PPI), the latter as prepulse inhibition of perceived stimulus intensity (PPIPSI). Both phenomena are used to study sensory gating in clinical and non-clinical populations, however little is known about their relationship. Here, we investigated 1) the possibility that cortical PPI and PPIPSI are associated, and 2) how they are affected by attentional load. Participants were tasked with comparing the intensity of an electric pulse presented alone versus one preceded 200 ms by a weaker electric prepulse (Experiment 1), or an acoustic pulse presented alone with one preceded 170 ms by a weaker acoustic prepulse (Experiment 2). A counting task (easy vs. hard) manipulating attentional load was included in Experiment 2. In both experiments, we observed a relationship between N1-P2 amplitude and perceived intensity, where greater cortical PPI was associated with a higher probability of perceiving the 'pulse with prepulse' as less intense. Moreover, higher attentional load decreased observations of PPIPSI but had no effect on N1-P2 amplitude. Based on the findings we propose that PPIPSI partially relies on the allocation of attentional resources towards monitoring cortical channels that process stimulus intensity characteristics such as the N1-P2 complex.

Evolving changes in cortical and subcortical excitability during movement preparation: A study of brain potentials and eye-blink reflexes during loud acoustic stimulation.

During preparation for action, the presentation of loud acoustic stimuli (LAS) can trigger movements at very short latencies in a phenomenon called the StartReact effect. It was initially proposed that a special, separate subcortical mechanism that bypasses slower cortical areas could be involved. We sought to examine the evidence for a separate mechanism against the alternative that responses to LAS can be explained by a combination of stimulus intensity effects and preparatory states. To investigate whether cortically mediated preparatory processes are involved in mediating reactions to LAS, we used an auditory reaction task where we manipulated the preparation level within each trial by altering the conditional probability of the imperative stimulus. We contrasted responses to non-intense tones and LAS and examined whether cortical activation and subcortical excitability and motor responses were influenced by preparation levels. Increases in preparation levels were marked by gradual reductions in reaction time (RT) coupled with increases in cortical activation and subcortical excitability - at both condition and trial levels. Interestingly, changes in cortical activation influenced motor and auditory but not visual areas - highlighting the widespread yet selective nature of preparation. RTs were shorter to LAS than tones, but the overall pattern of preparation level effects was the same for both stimuli. Collectively, the results demonstrate that LAS responses are indeed shaped by cortically mediated preparatory processes. The concurrent changes observed in brain and behavior with increasing preparation reinforce the notion that preparation is marked by evolving brain states which shape the motor system for action.

Engagement of the contralateral limb can enhance the facilitation of motor output by loud acoustic stimuli.

When intense sound is presented during light muscle contraction, inhibition of the corticomotoneuronal pathway is observed. During action preparation, this effect is reversed, with sound resulting in excitation of the corticomotoneuronal pathway. We investigated how the combined maintenance of a muscle contraction during preparation for a ballistic action impacts the magnitude of the facilitation of motor output by a loud acoustic stimulus (LAS), a phenomenon known as the StartReact effect. Participants executed ballistic wrist flexion movements and a LAS was presented simultaneously with the imperative signal in a subset of trials. We examined whether the force level or muscle used to maintain a contraction during preparation for the ballistic response impacted reaction time and/or the force of movements triggered by the LAS. These contractions were sustained either ipsilaterally or contralaterally to the ballistic response. The magnitude of facilitation by the LAS was greatest when low-force flexion contractions were maintained in the limb contralateral to the ballistic response during preparation. There was little change in facilitation when contractions recruited the contralateral extensor muscle or when they were sustained in the same limb that executed the ballistic response. We conclude that a larger network of neurons that may be engaged by a contralateral sustained contraction prior to initiation may be recruited by the LAS, further contributing to the motor output of the response. These findings may be particularly applicable in stroke rehabilitation, where engagement of the contralesional side may increase the benefits of a LAS to the functional recovery of movement.NEW & NOTEWORTHY The facilitation of reaction time, force, and vigor of a ballistic action by loud acoustic stimuli can be enhanced by the maintenance of a sustained contraction during preparation. This enhanced facilitation is observed when the sustained contraction is maintained with low force contralaterally and congruently with the ballistic response. This increased facilitation may be particularly applicable to rehabilitative applications of loud acoustic stimuli in improving the functional recovery of movement after neurological conditions such as stroke.

Premovement inhibition can protect motor actions from interference by response-irrelevant sensory stimulation.

KEY POINTS: Suppression of corticospinal excitability is reliably observed during preparation for a range of motor actions, leading to the belief that this preparatory inhibition is a physiologically obligatory component of motor preparation. The neurophysiological function of this suppression is uncertain. We restricted the time available for participants to engage in preparation and found no evidence for preparatory inhibition. The function of preparatory inhibition can be inferred from our findings that sensory stimulation can disrupt motor output in the absence of preparatory inhibition, but enhance motor output when inhibition is present. These findings suggest preparatory inhibition may be a strategic process which acts to protect prepared actions from external interference. Our findings have significant theoretical implications for preparatory processes. Findings may also have a pragmatic benefit in that acoustic stimulation could be used therapeutically to facilitate movement, but only if the action can be prepared well in advance. ABSTRACT: Shortly before movement initiation, the corticospinal system undergoes a transient suppression. This phenomenon has been observed across a range of motor tasks, suggesting that it may be an obligatory component of movement preparation. We probed whether this was also the case when the urgency to perform a motor action was high, in a situation where little time was available to engage in preparatory processes. We controlled the urgency of an impending motor action by increasing or decreasing the foreperiod duration in an anticipatory timing task. Transcranial magnetic stimulation (TMS; experiment 1) or a loud acoustic stimulus (LAS; experiment 2) were used to examine how corticospinal and subcortical excitability were modulated during motor preparation. Preparatory inhibition of the corticospinal tract was absent when movement urgency was high, though motor actions were initiated on time. In contrast, subcortical circuits were progressively inhibited as the time to prepare increased. Interestingly, movement force and vigour were reduced by both TMS and the LAS when movement urgency was high, and enhanced when movement urgency was low. These findings indicate that preparatory inhibition may not be an obligatory component of motor preparation. The behavioural effects we observed in the absence of preparatory inhibition were induced by both TMS and the LAS, suggesting that accessory sensory stimulation may disrupt motor output when such stimulation is presented in the absence of preparatory inhibition. We conclude that preparatory inhibition may be an adaptive strategy which can serve to protect the prepared motor action from external interference.

Cumulative distribution functions: An alternative approach to examine the triggering of prepared motor actions in the StartReact effect.

There has been much debate concerning whether startling sensory stimuli can activate a fast-neural pathway for movement triggering (StartReact) which is different from that of voluntary movements. Activity in sternocleidomastoid (SCM) electromyogram is suggested to indicate activation of this pathway. We evaluated whether SCM activity can accurately identify trials which may differ in their neurophysiological triggering and assessed the use of cumulative distribution functions (CDFs) of reaction time (RT) data to identify trials with the shortest RTs for analysis. Using recent data sets from the StartReact literature, we examined the relationship between RT and SCM activity. We categorised data into short/longer RT bins using CDFs and used linear mixed-effects models to compare potential conclusions that can be drawn when categorising data on the basis of RT versus on the basis of SCM activity. The capacity of SCM to predict RT is task-specific, making it an unreliable indicator of distinct neurophysiological mechanisms. Classification of trials using CDFs is capable of capturing potential task- or muscle-related differences in triggering whilst avoiding the pitfalls of the traditional SCM activity-based classification method. We conclude that SCM activity is not always evident on trials that show the early triggering of movements seen in the StartReact phenomenon. We further propose that a more comprehensive analysis of data may be achieved through the inclusion of CDF analyses. These findings have implications for future research investigating movement triggering as well as for potential therapeutic applications of StartReact.

Preparatory suppression and facilitation of voluntary and involuntary responses to loud acoustic stimuli in an anticipatory timing task.

In this study, we sought to characterize the effects of intense sensory stimulation on voluntary and involuntary behaviors at different stages of preparation for an anticipated action. We presented unexpected loud acoustic stimuli (LAS) at-rest and at three critical times during active movement preparation (-1,192, -392, and 0 ms relative to expected voluntary movement onset) to probe the state of the nervous system, and measured their effect on voluntary and involuntary motor actions (finger-press and eye-blink startle reflex, respectively). Voluntary responses were facilitated by LAS presented during active preparation, leading to earlier and more forceful responses compared to control and LAS at-rest. Notably, voluntary responses were significantly facilitated on trials where the LAS was presented early during preparation (-1,192 ms). Eye-blink reflexes to the LAS at -392 ms were significantly reduced and delayed compared to blinks elicited at other time-points, indicating suppression of sub-cortical excitability. However, voluntary responses on these trials were still facilitated by the LAS. The results provide insight into the mechanisms involved in preparing anticipatory actions. Induced activation can persist in the nervous system and can modulate subsequent actions for a longer time-period than previously thought, highlighting that movement preparation is a continuously evolving process that is susceptible to external influence throughout the preparation period. Suppression of sub-cortical excitability shortly before movement onset is consistent with previous work showing corticospinal suppression which may be a necessary step before the execution of any voluntary response.

Triggering Mechanisms for Motor Actions: The Effects of Expectation on Reaction Times to Intense Acoustic Stimuli.

Motor actions can be released much sooner than normal when the go-signal is of very high intensity (>100 dBa). Although statistical evidence from individual studies has been mixed, it has been assumed that sternocleidomastoid (SCM) muscle activity could be used to distinguish between two neural circuits involved in movement triggering. We summarized meta-analytically the available evidence for this hypothesis, comparing the difference in premotor reaction time (RT) of actions where SCM activity was elicited (SCM+ trials) by loud acoustic stimuli against trials in which it was absent (SCM- trials). We found ten studies, all reporting comparisons between SCM+ and SCM- trials. Our mini meta-analysis showed that premotor RTs are faster in SCM+ than in SCM- trials, but the effect can be confounded by the variability of the foreperiods employed. We present experimental data showing that foreperiod predictability can induce differences in RT that would be of similar size to those attributed to the activation of different neurophysiological pathways to trigger prepared actions. We discuss plausible physiological mechanisms that would explain differences in premotor RTs between SCM+ and SCM- trials.

Unexpected acoustic stimulation during action preparation reveals gradual re-specification of movement direction.

A loud acoustic stimulus (LAS) is often used as a tool to investigate motor preparation in simple reaction time (RT) tasks, where all movement parameters are known in advance. In this report, we used a LAS to examine direction specification in simple and choice RT tasks. This allowed us to investigate how the specification of movement direction unfolds during the preparation period. In two experiments, participants responded to the appearance of an imperative stimulus (IS) with a ballistic wrist force directed toward one of two targets. In probe trials, a LAS (120dBa) was delivered around the time of IS presentation. In Experiment 1, RTs in the simple RT task were faster when the LAS was presented, but the effect on the movement kinematics was negligible. In the Choice RT task, however, movement direction variability increased when the LAS was presented. In Experiment 2, when we primed movements toward one direction, our analyses revealed that the longer participants took to start a movement, the more accurate their responses became. Our results show not only that movement direction reprogramming occurs quickly and continuously, but also that LAS can be a valuable tool to obtain meaningful readouts of the motor system's preparatory state.

The facilitation of motor actions by acoustic and electric stimulation.

The presentation of a loud acoustic stimulus during the preparation of motor actions can both speed movement initiation and increase response vigor. Several recent studies have explored this phenomenon as a means to investigate the mechanisms and neural correlates of movement preparation. Here, we sought to determine the generality of this effect across sensory modalities, and in particular whether unexpected somatosensory stimulation can facilitate movements in a manner similar to loud sounds. We show that electric and acoustic stimuli can be similarly effective in inducing the early release of motor actions, in both reaction time and anticipatory timing tasks. Consistent with recent response activation models of motor preparation, we also demonstrate that increasing the intensity of electric stimuli induces both progressive decreases in reaction time and increases in response vigor. Additionally, we show that the early release of motor actions can be induced by electric stimuli targeting predominantly either muscle afferents or skin afferents. Finally, we show that simultaneous acoustic and electric stimulation leads to earlier releases of anticipatory actions than either unimodal stimulus. These findings may lead to new avenues for experimental and clinical exploitation of the effects of accessory sensory information on movement preparation and initiation.

The effects of preparation and acoustic stimulation on contralateral and ipsilateral corticospinal excitability.

A loud auditory stimulus (LAS) presented together with an imperative stimulus during preparation for motor actions can speed their initiation. The effects of LAS on corticospinal excitability (CSE), however, depend on the state of preparation of the motor system for action. CSE also depends on the brain hemisphere controlling the responding limb. Usually, CSE is increased just before movement onset in the hemisphere controlling the movement and inhibited on the other side. This study investigated the impact of LAS on CSE of the contralateral and ipsilateral hemispheres, while participants prepared for a voluntary abduction of the index finger. In Experiment 1, we attempted to identify the pattern of modulation of the ipsilateral cortex (resting side) by determining the time course of corticospinal changes in anticipatory timing actions using transcranial magnetic stimulation. In Experiment 2, we investigated the impact of LAS on the ipsilateral and contralateral CSE during anticipatory preparation. Results found no modulation of ipsilateral CSE during preparation, but indicate an increase in CSE after EMG onset on the acting limb. Moreover, we found that LAS presentation increased CSE on the contralateral side (active side).

The effect of attention on the release of anticipatory timing actions.

A loud auditory stimulus (LAS) presented during movement preparation can result in an earlier than normal movement onset. This effect had initially been assumed to be independent of the sensorial modality people attended to trigger their responses. In 2 experiments, we tested whether this assumption was warranted. In Experiment 1, we employed a timed response paradigm in which participants were cued in relation to the precise moment of movement onset of their motor responses. In the visual task, participants were cued about movement onset via visual cues on a monitor screen. In the auditory task, participants were cued about movement onset through tones delivered via headphones. During both tasks, we delivered an unexpected LAS 200 ms prior to movement onset. We found that the responses were initiated earlier by the LAS in the auditory task in relation to the visual task. In Experiment 2, we presented participants with a sequence of tones and flashes interleaved. The participants' task was to ignore either the tones or the flashes and make a movement in sync with the last tone or flash. The results showed that when participants had to ignore the task-irrelevant tones in the background, the early responses were much reduced. In contrast, when participants had to pay attention to the tones and ignore the flashes, the early release of anticipatory actions was robust. Our results indicate that attention to a specific sensorial modality can affect the early release of motor responses by LAS.

The early release of actions by loud sounds in muscles with distinct connectivity.

The presentation of an unexpected and loud auditory stimulus (LAS) during action preparation can trigger movement onset much sooner than normal. Recent research has attributed this effect to the activation of reticulospinal connections to the target muscles. To our knowledge, no studies have investigated the effects of LAS presentation in tasks requiring the simultaneous activation of muscles with different connectivity to motor areas of the brain. Here, we sought to establish the importance of muscle connectivity by asking participants to contract the orbicularis oris and abductor pollicis brevis muscles simultaneously. A LAS was randomly presented at 200 ms prior to the expected time of movement onset in an anticipatory timing task. We show that muscles controlled via bulbar connections to reticular formation can be triggered early by sound as much as muscles with spinal connections to the reticular formation.

Responses to loud auditory stimuli indicate that movement-related activation builds up in anticipation of action.

Previous research using a loud acoustic stimulus (LAS) to investigate motor preparation in reaction time (RT) tasks indicates that responses can be triggered well in advance of the presentation of an imperative stimulus (IS). This is intriguing given that high levels of response preparation cannot be maintained for long periods (≈ 200 ms). In the experiments reported here we sought to assess whether response-related activation increases gradually over time in simple RT tasks. In experiment 1, a LAS was presented at different times just prior to the presentation of the IS to probe the level of activation for the motor response. In experiment 2, the same LAS was presented at different times after the presentation of the IS. The results provide evidence that response-related activation does increase gradually in anticipation of the IS, but it remains stable for a short time after this event. The data display a pattern consistent with the response being triggering by the LAS, rather than a reaction to the IS.