Influence of kinesthetic motor imagery and effector specificity on the long-latency stretch response.

The long-latency "reflexive" response (LLR) following an upper limb mechanical perturbation is generated by neural circuitry shared with voluntary control. This feedback response supports many task-dependent behaviors and permits the expression of goal-directed corrections at latencies shorter than voluntary reaction time. An extensive body of literature has demonstrated that the LLR shows flexibility akin to voluntary control, but it has not yet been tested whether instruction-dependent LLR changes can also occur in the absence of an overt voluntary response. The present study used kinesthetic motor imagery (experiment 1) and instructed participants to execute movement with the unperturbed contralateral limb (experiment 2) to explore the relationship between the overt production of a voluntary response and LLR facilitation. Activity in stretched right wrist flexors were compared with standard "do not-intervene" and "compensate" conditions. Our findings revealed that on ~40% of imagery and ~50% of contralateral trials, a response occurred during the voluntary epoch in the stretched right wrist flexors. On these "leaked" trials, the early portion of the LLR (R2) was facilitated and displayed a similar increase to compensate trials. The latter half of the LLR (R3) showed further modulation, mirroring the patterns of voluntary epoch activity. By contrast, the LLR on "non-leaked" imagery and contralateral trials did not modulate. We suggest that even though a hastened voluntary response cannot account for all instruction-dependent LLR modulation, the overt execution of a response during the voluntary epoch in the same muscle(s) as the LLR is a prerequisite for instruction-dependent facilitation of this feedback response.NEW & NOTEWORTHY Using motor imagery and contralateral responses, we provide novel evidence that facilitation of the long-latency reflex (LLR) requires the execution of a response during the voluntary epoch. A high proportion of overt response "leaks" were found where the mentally simulated or mirrored response appeared in stretched muscle. The first half of the LLR was categorically sensitive to the appearance of leaks, whereas the latter half displayed characteristics closely resembling activity in the ensuing voluntary period.

Mechanical perturbations can elicit triggered reactions in the absence of a startle response.

Perturbations delivered to the upper limbs elicit reflexive responses in stretched muscle at short- (M1: 25-50 ms) and long- (M2: 50-100 ms) latencies. When presented in a simple reaction time (RT) task, the perturbation can also elicit a preprogrammed voluntary response at a latency (< 100 ms) that overlaps the M2 response. This early appearance of the voluntary response following a proprioceptive stimulus causing muscle stretch is called a triggered reaction. Recent work has demonstrated that a perturbation also elicits activity in sternocleidomastoid (SCM) over a time-course consistent with the startle response and it was, therefore, proposed that the StartReact effect underlies triggered reactions (Ravichandran et al., Exp Brain Res 230:59-69, 2013). The present work investigated whether perturbation-evoked SCM activity results from startle or postural control and whether triggered reactions can also occur in the absence of startle. In Experiment 1, participants "compensated" against a wrist extension perturbation. A prepulse inhibition (PPI) stimulus (known to attenuate startle) was randomly presented before the perturbation. Rather than attenuating SCM activity, the responses in SCM were advanced by the PPI stimulus. In Experiment 2, participants "assisted" a wrist extension perturbation. The perturbation did not reliably elicit startle but despite this, two-thirds of trials had RTs of less than 100 ms and the earliest responses began at ~ 70 ms. These findings suggest that SCM activity following a perturbation is the result of postural control and is not related to startle. Moreover, an overt startle response is not a prerequisite for the elicitation of a triggered reaction.

Preparation of timing structure involves two independent sub-processes.

The current study examined the processes involved in the preparation of sequencing and timing initiation for multi-component responses. In two experiments, participants performed a reaction time (RT) task involving a three key-press sequence with either a simple (isochronous) or complex (non-isochronous) timing structure. Conditions involved a precue that provided information about all features of the movement (simple RT), no features of the movement (choice RT), sequencing only, or timing structure only. When sequencing was precued, RT decreased significantly as compared to choice RT, indicative of advance preparation of sequencing. When timing was precued, RT decreased significantly compared to choice RT when the timing structure was simple, suggesting that some aspect of timing preparation can occur prior to the go stimulus. However, even when the timing structure was known in advance, RT was still affected by timing complexity, confirming that some aspect of timing preparation cannot occur until after the onset of the stimulus and thus occurs during the RT interval. To explain these findings, we propose a two-component model of preparation for the timing initiation structure in which timing selection occurs in advance but timing implementation must occur following the go signal. These results support and extend previous findings regarding the independence of the processes associated with response sequencing and timing initiation.

Investigation of timing preparation during response initiation and execution using a startling acoustic stimulus.

The purpose of the current study was to examine the processes involved in the preparation of timing during response initiation and execution through the use of a startling acoustic stimulus (SAS). In Experiment 1, participants performed a delayed response task in which a two key-press movement was to be initiated 200 ms after an imperative signal (IS) with either a short (200 ms) or long (500 ms) interval between key-presses. On selected trials, a SAS was presented to probe the preparation processes associated with the initiation delay and execution of the inter-key interval. The SAS resulted in a significant decrease in the initiation time, which was attributed to a speeding of pacemaker pulses used to time the delay interval, caused by an increased activation due to the SAS. Conversely, the SAS delayed the short inter-key interval, which was attributed to temporary interference with cortical processing. In Experiment 2, participants performed a 500-ms delayed response task involving two key-presses 200 ms apart. In this condition, the SAS resulted in significantly decreased initiation time and a delayed inter-key interval (p = .053). Collectively, these results support a different timeline for the preparation of the delay interval, which is thought to be prepared in advance of the IS, and the inter-key interval, which is thought to be prepared following the IS. This conclusion provides novel information with regard to timing preparation that is consistent with models in which response preparation, initiation, and execution are considered separate and dissociable processes.

Voluntary reaction time and long-latency reflex modulation.

Stretching a muscle of the upper limb elicits short (M1) and long-latency (M2) reflexes. When the participant is instructed to actively compensate for a perturbation, M1 is usually unaffected and M2 increases in size and is followed by the voluntary response. It remains unclear if the observed increase in M2 is due to instruction-dependent gain modulation of the contributing reflex mechanism(s) or results from voluntary response superposition. The difficulty in delineating between these alternatives is due to the overlap between the voluntary response and the end of M2. The present study manipulated response accuracy and complexity to delay onset of the voluntary response and observed the corresponding influence on electromyographic activity during the M2 period. In all active conditions, M2 was larger compared with a passive condition where participants did not respond to the perturbation; moreover, these changes in M2 began early in the appearance of the response (∼ 50 ms), too early to be accounted for by voluntary overlap. Voluntary response latency influenced the latter portion of M2, with the largest activity seen when accuracy of limb position was not specified. However, when participants aimed for targets of different sizes or performed movements of various complexities, reaction time differences did not influence M2 period activity, suggesting voluntary activity was sufficiently delayed. Collectively, our results show that while a perturbation applied to the upper limbs can trigger a voluntary response at short latency (<100 ms), instruction-dependent reflex gain modulation remains an important contributor to EMG changes during the M2 period.

Unified nature of bimanual movements revealed by separating the preparation of each arm.

Movement preparation of bimanual asymmetric movements is longer than bimanual symmetric movements in choice reaction time conditions, even when movements are cued directly by illuminating the targets (Blinch et al. in Exp Brain Res 232(3):947-955, 2014). This bimanual asymmetric cost may be caused by increased processing demands on response programming, but this requires further investigation. The present experiment tested the demands on response programming for bimanual movements by temporally separating the preparation of each arm. This was achieved by precuing the target of one arm before the imperative stimulus. We asked: What was prepared in advance when one arm was precued? The answer to this question would suggest which process causes the bimanual asymmetric cost. Advance movement preparation was examined by comparing reaction times with and without a precue for the left target and by occasionally replacing the imperative stimulus with a loud, startling tone (120 dB). A startle tone releases whatever movement is prepared in advance with a much shorter reaction time than control trials (Carlsen et al. in Clin Neurophysiol 123(1):21-33, 2012). Participants made bimanual symmetric and asymmetric reaching movements in simple and 2-choice reaction time conditions and a condition with a precue for the left target. We found a bimanual asymmetric cost in 2-choice conditions, and the asymmetric cost was significantly smaller when the left target was precued. These results, and the results from startle trials, suggest (1) that the precued movement was not fully programmed but partially programmed before the imperative stimulus and (2) that the asymmetric cost was caused by increased processing demands on response programming. Overall, the results support the notion that bimanual movements are not the sum of two unimanual movements; instead, the two arms of a bimanual movement are unified into a functional unit. When one target is precued, this critical unification likely occurs during response programming.

Facilitation and interference during the preparation of bimanual movements: contributions from starting locations, movement amplitudes, and target locations.

Symmetric, target-directed, bimanual movements take less time to prepare than asymmetric movements (Diedrichsen et al. in Cerebral Cortex 16(12):1729-1738, 2006; Heuer and Klein in Psychol Res 70(4):229-244, 2006b). The preparation savings for symmetric movements may be related to the specification of symmetric amplitudes, target locations, or both. The goals of this study were to determine which symmetric movement parameters facilitate the preparation of bimanual movements and to compare the size of the facilitation for different parameters. Thirty participants performed bimanual reaching movements that varied in terms of the symmetry/asymmetry of starting locations, movement amplitudes, and target locations. Reaction time savings were examined by comparing movements that had one symmetric parameter (and two asymmetric parameters) to movements with all asymmetric parameters. We observed significant savings (~10 ms) for movements with symmetric amplitudes and movements with symmetric target locations. Reaction time costs were examined by comparing movements that had two asymmetric parameters (and one symmetric parameter) to movements with all symmetric parameters. We observed significant reaction time costs (~13 ms) for all movements with asymmetric amplitudes. These results suggest that movement preparation is facilitated when amplitudes or target locations are symmetric and that movement preparation suffers interference when amplitudes are asymmetric. The relative importance of the three parameters to movement preparation, from most to least important, is movement amplitudes, target locations, and then starting locations. Interference with asymmetric amplitudes or target locations may be caused by cross-talk between concurrent processes of parameter specification during response programming.

Comparing movement preparation of unimanual, bimanual symmetric, and bimanual asymmetric movements.

The goal of this study was to determine the process or processes most likely to be involved in reaction-time costs for spatially cued bimanual reaching. We used reaction time to measure the cost of bimanual symmetric movements compared to unimanual movements (a bimanual symmetric cost) and the cost for bimanual asymmetric movements compared to symmetric movements (a bimanual asymmetric cost). The results showed that reaction times were comparable for all types of movements in simple reaction time; that is, there was neither a bimanual symmetric cost nor an asymmetric cost. Therefore, unimanual, bimanual symmetric, and bimanual asymmetric movements have comparable complexity during response initiation. In choice conditions, there was no bimanual symmetric cost but there was a bimanual asymmetric cost, indicating that the preparation of asymmetric movements is more complex than symmetric movements. This asymmetric cost is likely the result of interference during response programming.

Startle reveals independent preparation and initiation of triphasic EMG burst components in targeted ballistic movements.

Muscles involved in rapid, targeted movements about a single joint often display a triphasic [agonist (AG1)-antagonist (ANT)-agonist (AG2)] electromyographic (EMG) pattern. Early work using movement perturbations suggested that for short movements, the entire EMG pattern was prepared and initiated in advance (Wadman WJ, Dernier van der Gon JJ, Geuze RH, Mol CR. J Hum Mov Stud 5: 3-17, 1979), whereas more recent transcranial magnetic stimulation evidence indicates that the ANT may be programmed separately (MacKinnon CD, Rothwell JC. J Physiol 528: 633-645, 2000) with execution of the bursts occurring serially (Irlbacher K, Voss M, Meyer BU, Rothwell JC. J Physiol 574: 917-928, 2006). The purpose of the current study was to investigate the generation of triphasic EMG bursts for movements of different amplitudes. In experiment 1, participants performed rapid elbow extension movements to 20° and 60° targets, and on some trials, a startling acoustic stimulus (SAS), which is thought to trigger prepared motor commands at short latency, was delivered at the onset of AG1. For short movements, this perturbation elicited ANT and AG2 early, suggesting the agonist and antagonist bursts may have been programmed independently. In contrast, the same manipulation did not disrupt EMG timing parameters for the long movements, raising the possibility that ANT and AG2 were not fully programmed in advance of movement onset. In experiment 2, an SAS was delivered later in the movement, which produced early onset of both ANT and AG2. We propose that the triphasic pattern is executed serially but believe the trigger signal for initiating the ANT burst occurs not in relation to the AG1 burst, but rather in close temporal proximity to the expected onset of ANT.

Unconscious and out of control: subliminal priming is insensitive to observer expectations.

We asked whether the influence of an invisible prime on movement is dependent on conscious movement expectations. Participants reached to a central target, which triggered a directional prime-mask arrow sequence. Participants were instructed that the visible arrows (masks) would most often signal a movement modification in a specific (biased) direction. Kinematic analyses revealed that responses to the visible mask were influenced by participants' intentional bias, as movements were fastest when the more probable mask was displayed. In addition, responses were influenced by the invisible prime without regard to its relationship to the more probable mask. Analysis of the time of initial trajectory modifications revealed that both primes influenced responses in a similar manner after accounting for participants' bias. These results imply that invisible stimuli automatically activate their associated responses and that unconscious priming of the motor system is insensitive to the conscious expectations of the participant making the pointing movements.

Startle decreases reaction time to active inhibition.

In reaction time (RT) tasks where fast ballistic movements are required, the requisite action is generally preplanned to enable the quickest responses. When a loud acoustic stimulus (e.g., >120 dB) that elicits a startle response is presented during the preplanning phase, the movement is triggered involuntarily and at a sufficiently short enough latency to discount normal cortical initiation processes. It has been suggested that the startle triggers the action by providing sufficient additional activation to surpass the initiation threshold. It is unclear, however, whether similar RT shortening due to startle would occur in the absence of an excitatory motor output. Thus, in the current study, participants performed a flexion force offset (i.e., inhibition) task within a simple RT paradigm. A startling acoustic stimulus (SAS) was presented in place of the usual "go" signal on several trials. Results from startle trials showed that the inhibitory command could be elicited substantially earlier by an SAS (latency of ~78 ms) compared to control trials (120 ms). This suggests active inhibition is preprogrammed and can be triggered early by startle in similar way to traditional "excitatory" tasks. Additionally, early startle-related EMG activity superimposed with the triggered offset suggests that the nature of the inhibitory command used in the current experiment involves the active suppression of ongoing motor output.

Investigation of stimulus-response compatibility using a startling acoustic stimulus.

We investigated the processes underlying stimulus-response compatibility by using a lateralized auditory stimulus in a simple and choice reaction time (RT) paradigm. Participants were asked to make either a left or right key lift in response to either a control (80dB) or startling (124dB) stimulus presented to either the left ear, right ear, or both ears. In the simple RT paradigm, we did not find a compatibility effect for either control or startle trials but did find a right-ear advantage which we attribute to anatomical asymmetry of auditory pathways. In the choice RT paradigm, we found compatibility effects for both startle and control trials as well a high incidence of error for contralateral stimulus-response mapping. We attribute these results to automatic activation of the ipsilateral response, which must then be inhibited prior to initiation of the correct response. The presence of compatibility effects for startle trials also suggest that similar pathways are being used to initiate movements in a choice RT situation, as opposed to involuntary triggering that is thought to occur in a simple RT situation.

The adaptability of self-action perception and movement control when the limb is passively versus actively moved.

Research suggests that perceptual experience of our movements adapts together with movement control when we are the agents of our actions. Is this agency critical for perceptual and motor adaptation? We had participants view cursor feedback during elbow extension-flexion movements when they (1) actively moved their arm, or (2) had their arm passively moved. We probed adaptation of movement perception by having participants report the reversal point of their unseen movement. We probed adaptation of movement control by having them aim to a target. Perception and control of active movement were influenced by both types of exposure, although adaptation was stronger following active exposure. Furthermore, both types of exposure led to a change in the perception of passive movements. Our findings support the notion that perception and control adapt together, and they suggest that some adaptation is due to recalibrated proprioception that arises independently of active engagement with the environment.

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.

Reach adaptation to online target error.

Magescas et al. (Exp Brain Res 193:337-350, 2009) recently suggested that online error, unlike terminal error, does not lead to reach adaptation. The present study re-examines adaptation to online target error, but uses a small target perturbation and eliminates online vision of the limb, factors that may affect adaptation. We compared 3 groups: terminal error, online error, and control. All groups completed a pretest, exposure, and posttest phase. Participants made look-and-point movements to a target, and we examined how repeated rightward target perturbations during the exposure phases of the experimental groups influenced reaches to a stationary target in the posttest. Exposure phases of each group contained an equal number of interleaved look-and-point and look-only trials, the latter of which were designed to inhibit build-up of saccadic adaptation in the online error group. On look-and-point trials the target either disappeared at saccade onset and then re-appeared 3.75 cm to the right when the hand landed (terminal error group), immediately jumped right by 3.75 cm at saccade onset and remained lit throughout the saccade and reach (online error group), or remained lit but stationary throughout the saccade and reach (control group). In all groups, vision of the limb was only provided at the start and end of the reach. Our results show that both the terminal error and the online error groups developed significant aftereffects. It appears, therefore, that online error can produce reach adaptation.

Default motor preparation under conditions of response uncertainty.

In a choice reaction time (RT) paradigm, providing partial advance information (a precue) about the upcoming response has been shown to decrease RT, presumably due to preprogramming of the precued parameters. When advance information about a particular aspect of a movement is provided (precued), several different strategies might be used to prepare the motor system during the foreperiod. For example, in studies where response preparation time was manipulated, precues were provided specifying the required arm and direction but movement amplitude was left uncertain. In this case it was shown that a default movement was preprogrammed whose amplitude was intermediate between the alternatives (Favilla et al. in Exp Brain Res 75(2):280-294, 1989, Exp Brain Res 79(3):530-538, 1990; Ghez et al. in Exp Brain Res 115(2):217-233, 1997). However, this strategy did not appear to be used in a RT task since there was an absence of online adjustments to movement. Therefore, it appeared movements were not initiated until all parameters had been correctly specified and programmed by the nervous system (Bock and Arnold in Exp Brain Res 90:(1):209-216, 1992). The present study reinvestigated the notion of a default movement preparation strategy in a choice RT paradigm, employing the triggering effect of a startling acoustic stimulus. On control trials (80 dB imperative stimulus), the movements were initiated toward the correct targets. Providing a startle stimulus (124 dB) resulted in the early initiation of a "default" movement whose amplitude fell in between the potential response alternatives. Thus, the current experiment found behavioral evidence of default intermediate-amplitude movement preparation as a strategy under conditions of response amplitude uncertainty.

Bimanual reaches with symbolic cues exhibit errors in target selection.

We examined the movement trajectories of symmetric and asymmetric bimanual reaches to targets specified by direct spatial cues and by indirect symbolic cues. Symbolically cued asymmetric reaches have been shown to exhibit longer reaction times compared with symmetric reaches, whereas no such reaction time cost is observed when targets are spatially cued--a pattern thought to implicate increased demands on response selection (Diedrichsen et al. in Psychol Sci 12(6):493-498, 2001). As symbolically cued reaches impose greater demands on cognitive visuomotor translation than spatially cued reaches (Diedrichsen et al. in Cereb Cortex 16(12):1729-1738, 2006), we asked whether bimanual movements exhibit more spatial coupling with symbolic cues than with spatial cues. Participants made bimanual symmetric and asymmetric reaches to short- and long-distance targets cued either symbolically or spatially. We replicated the reaction time cost for symbolically cued asymmetric movements. A subset of these asymmetric reaches also showed large trajectory modulations. It appeared that this subset had been incorrectly prepared and the movements required of the left and right arms had been switched. No such errors in target selection were observed when targets were spatially cued. In contrast to the reaction time cost and errors in selection for symbolically cued movements, we observed little evidence of increased spatial coupling with symbolic cues when movements were initiated towards the correct targets. We conclude that cognitive visuomotor translation demands during response selection increases bimanual coupling at the level of response selection (reaction time cost, errors in target selection) but not at the level of movement execution (spatial coupling).

Reach adaptation to explicit vs. implicit target error.

The adaptation of reaching movements has typically been investigated by either distorting visual feedback of the reaching limb or by distorting the forces acting upon the reaching limb. Here, we investigate reach adaptation when error is created by systematically perturbing the target of the reach rather than the limb itself (Magescas and Prablanc in J Cogn Neurosci 18: 75-83, 2006). Specifically, we investigate how adaptation is affected by (1) the timing of the perturbation with respect to the movement of the eye and the hand and (2) participant awareness of the perturbation. In Experiment 1, participants looked and pointed to a target that disappeared either at the onset of their eye movement or shortly after their eye movement and then reappeared, displaced to the right, at the completion of the reach. In Experiment 2, we made the target displacement more explicit by leaving the target at its initial location until the end of the reach, at which point it was displaced to the right. In Experiment 3, we extinguished the target at the onset of the eye movement but also informed participants about the presence and magnitude of the perturbation. In the no-feedback post-test phase, participants for whom the target disappeared during the reach demonstrated much stronger aftereffects of the perturbation, misreaching to the right, whereas participants for whom the target stayed on until reach completion demonstrated rapid extinction of rightward misreaching. Furthermore, participants who were informed about the target perturbation exhibited faster de-adaptation than those who were not. Our results suggest that adaptation to a target displacement is contingent on the explicitness of the target perturbation, whether this is achieved by manipulating stimulus timing or instruction.

Implicit motor learning from target error during explicit reach control.

Many studies have shown adapted reaching in the face of altered visual feedback. These studies typically involve iterative corrections to the error induced by the perturbation until relatively normal performance is achieved. Here, we investigate whether adaptation (indexed by aftereffects) can occur when direct corrections to a target are inhibited by giving participants an explicit reach task. During the exposure phase of our study, participants were instructed to undershoot a target that imperceptibly moved between movement onset and movement end. The size of the target displacement was gradually increased, while the instructed undershoot distance was equivalently increased, such that participants were, unknowingly, aiming to the same location throughout exposure. When participants were subsequently instructed to aim at the target during the post-test, they overshot the target, suggesting that adaptation had occurred in the presence of an explicit task and in the absence of direct corrections to the target perturbation.