Dana Maslovat

Considerations for the use of a startling acoustic stimulus in studies of motor preparation in humans

Recent studies have used a loud (> 120 dB) startle-eliciting acoustic stimulus as a probe to investigate early motor response preparation in humans. The use of a startle in these studies has provided insight into not only the neurophysiological substrates underlying motor preparation, but also into the behavioural response strategies associated with particular stimulus-response sets. However, as the use of startle as a probe for preparation is a relatively new technique, a standard protocol within the context of movement paradigms does not yet exist. Here we review the recent literature using startle as a probe during the preparation phase of movement tasks, with an emphasis on how the experimental parameters affect the results obtained. Additionally, an overview of the literature surrounding the startle stimulus parameters is provided, and factors affecting the startle response are considered. In particular, we provide a review of the factors that should be taken into consideration when using a startling stimulus in human research.

Motor preparation and the effects of practice: Evidence from startle.

To examine sequential movement preparation, participants practiced unimanual movements that differed in amplitude and number of elements for 4 days in either a simple (Experiment 1) or choice (Experiment 2) reaction time (RT) paradigm. On Day 1 and 4, a startling stimulus was used to probe the preparation process. For simple RT, we found increased premotor RT for the two component movement during control trials on Day 1, which was minimized with practice. During startle trials, all movements were triggered at a short latency with similar consistency to control trials, suggesting full advance preparation of all movements. For choice RT, we also found increased premotor RT for control trials for the two component movement. As advance preparation could not occur, the startling stimulus did not trigger any of the movements. We hypothesized that complexity may relate to the neural commands needed to produce the movement, rather than a sequencing requirement.

Feedback Effects on Learning a Novel Bimanual Coordination Pattern: Support for the Guidance Hypothesis

The authors tested specificity and the guidance hypothesis by examining the effects of continuous or discrete concurrent feedback during acquisition, retention, and transfer of a 90° phase offset bimanual coordination pattern. The authors tested both groups immediately following acquisition, 1 week later under retention conditions (i.e., identical feedback as acquisition) and under transfer conditions with a change in feedback (i.e., discrete to continuous or vice versa) and with no feedback. Acquisition results revealed superior performance by the continuous feedback group. However, during immediate transfer conditions, the continuous group showed decreased pattern accuracy and stability, whereas the discrete group improved its performance. These results support the guidance hypothesis, as the participants with a high amount of feedback in acquisition became reliant on the feedback and could not adapt their learning to a new situation. These results also show partial support for the specificity of practice hypothesis as the continuous group was only able to mimic their acquisition performance under identical conditions as practice. Practice specificity effects were not found for the discrete group, as performance was not negatively affected with a change or removal of afferent information.

Response preparation changes following practice of an asymmetrical bimanual movement

The purpose of the current study was to examine the effects of practice on the advance preparation of an asymmetrical bimanual movement. Participants performed 170 trials of a discrete bimanual aiming movement where the right arm moved twice the amplitude of the left, in response to an auditory “go” signal. During three of the first and last ten trials, the “go” signal was replaced with a startle (124 dB) stimulus, which is thought to trigger a prepared movement. Startle and non-startle (control) trials from early and late practice were compared on various kinematic and EMG measures. Results indicated that it is possible to pre-program a bimanual asymmetrical movement, and that advance preparation of movement amplitude changes with practice. Evidence was also provided that the different amplitude movements were performed using similar EMG timing between limbs, while adjusting the relative ratio of EMG amplitude. Furthermore, learning of the task appeared to be related to the ability to prepare the correct asymmetrical EMG amplitudes rather than changing the timing of the EMG pattern.

Anchoring strategies for learning a bimanual coordination pattern

Anchoring has been defined as synchronizing a point in a movement cycle with an external stimulus (W. D. Byblow, R. G. Carson, & D. Goodman, 1994). Previously, investigators have examined anchoring during in-phase and antiphase movements. The present authors examined anchoring during acquisition of a novel bimanual coordination pattern. Participants performed a 90° pattern at 1 Hz, with a 2- or 4-Hz metronome. No group differences were found in pattern performance; however, the 4-Hz group developed more consistent anchoring relative to the metronome. Mechanical anchor-point variability differed by hand, position (midpoint vs. endpoint), and direction (flexion vs. extension) but not by metronome frequency. Those results support and extend previous findings but leave unanswered questions regarding the benefits and effectiveness of anchoring during a 90° pattern.

Responses to startling acoustic stimuli indicate that movement‐related activation is constant prior to action: a replication with an alternate interpretation

A recent study by Marinovic et al. (J. Neurophysiol., 2013, 109: 996–1008) used a loud acoustic stimulus to probe motor preparation in a simple reaction time (RT) task. Based on decreasing RT latency and increases in motor output measures as the probe stimulus approached the “go” stimulus, the authors concluded that response‐related activation increased abruptly 65 ms prior to the imperative stimulus, a result in contrast to previous literature. However, this study did not measure reflexive startle activity in the sternocleidomastoid (SCM) muscle, which has been used to delineate between response triggering by a loud acoustic stimuli and effects of stimulus intensity and/or intersensory facilitation. Due to this methodological limitation, it was unclear if the data accurately represented movement‐related activation changes. In order to provide a measure as to whether response triggering occurred on each trial, the current experiment replicated the study by Marinovic et al., with the collection of muscle activation in the SCM. While the replication analyses involving all trials confirmed similar results to those reported by Marinovic et al., when data were limited to those in which startle‐related SCM activation occurred, the results indicated that movement‐related activation is constant in the 65 ms prior to action initiation. The difference between analyses suggests that when SCM activation is not considered, results may be confounded by trials in which the probe stimulus does not trigger the prepared response. Furthermore, these results provide additional confirmation that reflexive startle activation in the SCM is a robust indicator of response triggering by a loud acoustic stimulus.

Anodal transcranial direct current stimulation applied over the supplementary motor area delays spontaneous antiphase-to-in-phase transitions

Coordinated bimanual oscillatory movements often involve one of two intrinsically stable phasing relationships characterized as in-phase (symmetrical) or antiphase (asymmetrical). The in-phase mode is typically more stable than antiphase, and if movement frequency is increasing during antiphase movements, a spontaneous transition to the in-phase pattern occurs. There is converging neurophysiological evidence that the supplementary motor area (SMA) plays a critical role in the successful performance of these patterns, especially during antiphase movements. We investigated whether modulating the excitability of the SMA via offline transcranial direct current stimulation (tDCS) would delay the onset of anti-to-in-phase transitions. Participants completed two sessions (separated by ∼48 h), each consisting of a pre- and post-tDCS block in which they performed metronome-paced trials of rhythmic in- and antiphase bimanual supination-pronation movements as target oscillation frequency was systematically increased. Anodal or cathodal tDCS was applied over the SMA between the pre- and post-tDCS blocks in each session. Following anodal tDCS, participants performed the antiphase pattern with increased accuracy and stability and were able to maintain the coordination pattern at a higher oscillation frequency. Antiphase performance was unchanged following cathodal tDCS, and neither tDCS polarity affected the in-phase mode. Our findings suggest increased SMA excitability induced by anodal tDCS can improve antiphase performance and adds to the accumulating evidence of the pivotal role of the SMA in interlimb coordination.

Subcortical motor circuit excitability during simple and choice reaction time.

The purpose of the current study was to examine the relationship between movement preparation and excitability of subcortical motor circuits, as measured by the reflexive response to a startling acoustic stimulus. We compared the size and incidence of activation in the sternocleidomastoid (startle indicator) from participants completing either a simple or choice reaction time (RT) task. Consistent with predictions, results indicated that the startle reflex habituated after several presentations of the SAS for the choice RT group but not for the simple RT group, which we attributed to advance motor preparatory processes involved in a simple RT task. Additionally, when participants from the choice RT group were put into a simple RT condition, the startle reflex response returned to nonhabituated levels. We conclude that the increased corticospinal activation associated with advance preparation may also result in increased subcortical activation, accounting for the observed lack of habituation to a startling stimulus in simple RT.

Evidence for a response preparation bottleneck during dual-task performance: effect of a startling acoustic stimulus on the psychological refractory period.

The present study was designed to investigate the mechanism associated with dual-task interference in a psychological refractory period (PRP) paradigm. We used a simple reaction time paradigm consisting of a vocal response (R1) and key-lift task (R2) with a stimulus onset asynchrony (SOA) between 100ms and 1500ms. On selected trials we implemented a startling acoustic stimulus concurrent with the second stimulus to determine if we could involuntarily trigger the second response. Our results indicated that the PRP delay in the second response was present for both control and startle trials at short SOAs, suggesting the second response was not prepared in advance. These results support a response preparation bottleneck and can be explained via a neural activation model of preparation. In addition, we found that the reflexive startle activation was reduced in the dual-task condition for all SOAs, a result we attribute to prepulse inhibition associated with dual-task processing.

Motor preparation of spatially and temporally defined movements: evidence from startle

Previous research has shown that the preparation of a spatially targeted movement performed at maximal speed is different from that of a temporally constrained movement (Gottlieb et al. 1989b). In the current study, we directly examined preparation differences in temporally vs. spatially defined movements through the use of a startling stimulus and manipulation of the task goals. Participants performed arm extension movements to one of three spatial targets (20°, 40°, 60°) and an arm extension movement of 20° at three movement speeds (slow, moderate, fast). All movements were performed in a blocked, simple reaction time paradigm, with trials involving a startling stimulus (124 dB) interspersed randomly with control trials. As predicted, spatial movements were modulated by agonist duration and timed movements were modulated by agonist rise time. The startling stimulus triggered all movements at short latencies with a compression of the kinematic and electromyogram (EMG) profile such that they were performed faster than control trials. However, temporally constrained movements showed a differential effect of movement compression on startle trials such that the slowest movement showed the greatest temporal compression. The startling stimulus also decreased the relative timing between EMG bursts more for the 20° movement when it was defined by a temporal rather than spatial goal, which we attributed to the disruption of an internal timekeeper for the timed movements. These results confirm that temporally defined movements were prepared in a different manner from spatially defined movements and provide new information pertaining to these preparation differences.