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.

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.

Acoustic stimulation increases implicit adaptation in sensorimotor adaptation.

Sensorimotor adaptation is an important part of our ability to perform novel motor tasks (i.e., learning of motor skills). Efforts to improve adaptation in healthy and clinical patients using non-invasive brain stimulation methods have been hindered by inter-individual and intra-individual variability in brain susceptibility to stimulation. Here, we explore unpredictable loud acoustic stimulation as an alternative method of modulating brain excitability to improve sensorimotor adaptation. In two experiments, participants moved a cursor towards targets, and adapted to a 30º rotation of cursor feedback, either with or without unpredictable acoustic stimulation. Acoustic stimulation improved initial adaptation to sensory prediction errors in Study 1, and improved overnight retention of adaptation in Study 2. Unpredictable loud acoustic stimulation might thus be a potent method of modulating sensorimotor adaptation in healthy adults.

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.

Neural gain induced by startling acoustic stimuli is additive to preparatory activation.

Loud acoustic stimuli presented during movement preparation can shorten reaction time and increase response forcefulness. We examined how efferent connectivity of an agonist muscle to reticulospinal and corticospinal pathways, and the level of prepared movement force, affect reaction time and movement execution when the motor response is triggered by an intense acoustic stimulus. In Experiment 1, participants executed ballistic wrist flexion and extension movements of low and high force in response to visual stimuli. A loud acoustic stimulus (LAS; 105 dBa) was presented simultaneously with the visual imperative stimulus in probe trials. In Experiment 2, participants executed ballistic wrist flexion movements ranging from 10%-50% of maximum voluntary contraction with a LAS presented in probe trials. The shortening of response initiation was not affected by movement type (flexion or extension) or prepared movement force. Enhancement of response magnitude, however, was proportionally greater for low force movements and for the flexor muscle. Changes in peak force induced by the intense acoustic stimulus indicated that the neural activity introduced to motor program circuits by acoustic stimulation is additive to the voluntary neural activity that occurs due to movement preparation, rather than multiplicative.

Grasping at laws: Speed-accuracy trade-offs in manual prehension.

Most of human performance is subject to speed-accuracy trade-offs. For spatially constrained aiming, the trade-off is often said to take the specific form of Fitts' law, in which movement duration is predicted from a single factor combining target distance and target size. However, efforts to extend this law to the three-dimensional context of reaching to grasp (prehension) have had limited success. We suggest that there are potentially confounding influences in standard grasping, and we introduce a novel task to regularize the direction of approach and to eliminate the influences of nearby surfaces. In six participants, we examined speed-accuracy trade-offs for prehension, manipulating the depth (in the plane of the reach), height (orthogonal to the reach), and width (the grasped dimension) of the target object independently. We obtained lawful relationships that were consistent at the group and individual levels. It took longer to reach for more distant objects, and more time was allowed when placing the fingers on a contact surface smaller in either depth or height. More time was taken to grasp wider objects, but only beyond a critical width that varied between individuals. These speed-accuracy trade-offs showed substantial departures from Fitts' law, and were well described by a two-factor model in which reach distance and object size have separate influences on movement duration. We discuss empirical and theoretical reasons for preferring a two-factor model, and we propose that this may represent the most general form of speed-accuracy trade-off, not only for grasping but also for other spatially constrained aiming tasks. (PsycINFO Database Record

Intercepting accelerated moving targets: effects of practice on movement performance.

When performing a rapid manual interception, targets moving under constant motion are often intercepted with greater accuracy when compared to targets moving under accelerated motion. Usually, accelerated targets are timed too late and decelerating ones too early. The present experiment sought to investigate whether these differences in performance when intercepting targets moving under constant and accelerated motions change after a short period of practice. The task involved striking targets that moved along a straight track by moving forward a manipulandum that moved along a slide perpendicular to the target's motion. Participants were allocated to one of the three experimental groups, defined according to the type of motion of the moving targets: constant speed, constant acceleration, and constant deceleration. Results showed that after some practice participants were able to intercept (positive and negative) accelerating moving targets as accurately as constant speed targets. These results suggest that people might be able to learn how to intercept accelerating targets, corroborating the results of some recent studies.

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.

Corticospinal modulation induced by sounds depends on action preparedness.

A loud acoustic stimulus (LAS) presented during movement preparation can induce an early release of the prepared action. Because loud sound has been found to have an inhibitory effect on motor cortex excitability, it is possible that the motor cortex plays little role in the early release of prepared responses. We sought to shed new light on this suggestion by probing changes in corticospinal excitability after LAS presentation during preparation for an anticipatory action. Unexpectedly, we show that the changes in corticospinal excitability after LAS presentation are not fixed. Based on the magnitude of motor-evoked potentials elicited by transcranial magnetic and electric stimulation of the motor cortex, we demonstrate that the effects of auditory stimuli on corticospinal excitability depend on the level of readiness for action: inhibition in early preparation and facilitation close to movement onset. We also show that auditory stimuli can regulate intracortical excitability by increasing intracortical facilitation and reducing short-interval intracortical inhibition. Together, these findings indicate that, at least in part, the early release of motor responses by auditory stimuli involves the motor cortex.

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.

Corticospinal excitability during preparation for an anticipatory action is modulated by the availability of visual information.

To intercept rapidly moving objects, people must predict the right time to initiate their actions. The timing of movement initiation in interceptions is thought to be determined when a perceptual variable specifying time to contact reaches a criterion value. If a response needs to be aborted, the performer must make a decision before this moment. It has been recently shown that the minimal time to suppress an anticipatory action takes longer during motion extrapolation than during continuous visual information. In experiment 1, we sought to determine whether or not the availability of visual information would 1) affect the latency to inhibit an anticipatory action, and 2) modulate the level of excitability in the motor cortex (M1). The behavioral results showed that the absence of visual information prolonged the latency to stop the movement as previously reported. The neurophysiological data indicated that corticospinal excitability levels were affected by the availability of visual information. In experiment 2, we sought to verify whether corticospinal excitability levels would also differ between the two visual conditions when the task did not involve response suppression. The results of experiment 2 indicated that excitability levels did not differ between visual conditions. Overall, our findings indicated that the buildup of motor activation can also play a role in determining different latencies to inhibit an anticipatory action. They also suggest that the buildup of motor activation in the corticospinal pathways can be strategically modulated to the requirements of the task during continuous visual information.

Continuous priming effects on discrete response choices.

When primed by backward-masked, target-like stimuli, discrete responses (e.g. button presses) to simple visual targets can be slower when prime and target match (compatible) than when they do not (incompatible). The current study investigated the nature of the stimulus-response mapping underlying this negative compatibility effect (NCE). Discrete left-right responses to arrow targets were primed with arrows oriented in one of 16 directions. Responses were either a standard button press or a 10 cm movement on a graphics tablet. Both tasks showed an identical NCE; importantly, reaction times in both tasks decreased smoothly as the angular distance between prime and target increased (i.e. as compatibility decreased), with the largest NCE evident between the extreme cases (prime-target distances of 0 degrees and 180 degrees ). Primes exerted an effect on the required response in proportion to the amount of overlap (reflecting population vector coding). The mapping between the priming stimulus and response is continuous, not categorical.

The effect of priming on interceptive actions.

Time constraints in ball sports encourage players to take advantage of any relevant advance information available to prepare their actions. Advance information, therefore, can serve to prime movement parameters (e.g. movement direction) and reduce the amount of time required to prepare the upcoming movement. Regularly, however, players face situations in which the information used to prepare the action turns out to be outdated just prior to movement initiation and the prepared action needs to be changed as soon as possible. The aim of the experiment presented here was to determine whether the priming effect, generally reported for reaction time tasks, could be generalised to interceptive actions. A secondary aim was to examine the strategies employed by the participants to cope with valid, invalid, or no advance information. The results indicate that, when available, the participants used advance information to prepare their movements. More specifically, in comparison with valid advance information, hit rate and spatial accuracy were reduced when the participants had no advance information and were even smaller when the information conveyed was invalid. The results also suggest that in the absence of valid advance information, the strategies employed to intercept the moving target were tuned to the time remaining until the interception was due to occur.

Delayed inhibition of an anticipatory action during motion extrapolation.

BACKGROUND: Continuous visual information is important for movement initiation in a variety of motor tasks. However, even in the absence of visual information people are able to initiate their responses by using motion extrapolation processes. Initiation of actions based on these cognitive processes, however, can demand more attentional resources than that required in situations in which visual information is uninterrupted. In the experiment reported we sought to determine whether the absence of visual information would affect the latency to inhibit an anticipatory action. METHODS: The participants performed an anticipatory timing task where they were instructed to move in synchrony with the arrival of a moving object at a determined contact point. On 50% of the trials, a stop sign appeared on the screen and it served as a signal for the participants to halt their movements. They performed the anticipatory task under two different viewing conditions: Full-View (uninterrupted) and Occluded-View (occlusion of the last 500 ms prior to the arrival at the contact point). RESULTS: The results indicated that the absence of visual information prolonged the latency to suppress the anticipatory movement. CONCLUSION: We suggest that the absence of visual information requires additional cortical processing that creates competing demand for neural resources. Reduced neural resources potentially causes increased reaction time to the inhibitory input or increased time estimation variability, which in combination would account for prolonged latency.

The time course of direction specification in brief interceptive actions.

In fastball sports such as baseball and tennis people are required to produce accurate responses following brief observations of the ball. This limits the time available to prepare the movement. To cope with constrained viewing periods which precede the interception of fast approaching balls, performers are likely to prepare their responses in advance. Although motor preparation may begin before the moving object is seen, accuracy requires that certain program parameters are determined from observations of the target. The aim of the experiment reported here was to determine the last moment at which information about the direction of the target can be incorporated into a motor program. The empirical protocol used in this study allowed us to examine whether new direction information is incorporated discretely or continuously into the program during short intervals prior to movement onset (MO) - the preparation interval. Participants were trained to hit moving targets at two directions with movements of a specific duration (180 ms). This method permitted an estimate of MO. Preparation intervals were controlled by issuing a stimulus cue for movement direction at various times prior to the estimated MO. Results showed that direction information could be fully incorporated into the program with a preparation interval as brief as 250 ms. In addition, the results indicated that direction was specified predominantly in a discrete fashion even at short preparation intervals.

Real-time error detection but not error correction drives automatic visuomotor adaptation.

We investigated the role of visual feedback of task performance in visuomotor adaptation. Participants produced novel two degrees of freedom movements (elbow flexion-extension, forearm pronation-supination) to move a cursor towards visual targets. Following trials with no rotation, participants were exposed to a 60 degrees visuomotor rotation, before returning to the non-rotated condition. A colour cue on each trial permitted identification of the rotated/non-rotated contexts. Participants could not see their arm but received continuous and concurrent visual feedback (CF) of a cursor representing limb position or post-trial visual feedback (PF) representing the movement trajectory. Separate groups of participants who received CF were instructed that online modifications of their movements either were, or were not, permissible as a means of improving performance. Feedforward-mediated performance improvements occurred for both CF and PF groups in the rotated environment. Furthermore, for CF participants this adaptation occurred regardless of whether feedback modifications of motor commands were permissible. Upon re-exposure to the non-rotated environment participants in the CF, but not PF, groups exhibited post-training aftereffects, manifested as greater angular deviations from a straight initial trajectory, with respect to the pre-rotation trials. Accordingly, the nature of the performance improvements that occurred was dependent upon the timing of the visual feedback of task performance. Continuous visual feedback of task performance during task execution appears critical in realising automatic visuomotor adaptation through a recalibration of the visuomotor mapping that transforms visual inputs into appropriate motor commands.

Preparation and inhibition of interceptive actions.

Two experiments aimed to provide an estimate of the last moment at which visual information needs to be obtained in order for it to be used to initiate execution of an interceptive movement or to withhold execution of such a movement. In experiment 1, we sought to estimate the minimum time required to suppress the movement when the participants were first asked to intercept a moving target. In experiment 2, we sought to determine the minimum time required to initiate an interceptive movement when the participants were initially asked to keep stationary. Participants were trained to hit moving targets using movements of a pre-specified duration. This permitted an estimate of movement onset (MO) time. In both experiments the requirement to switch from one prepared course of action to the other was indicated by changing the colour of the moving target at times prior to the estimated MO. The results of the experiments showed that the decision to execute or suppress the interception must be made no less than about 200 ms before MO.