Name: an emerging target paradigm to evoke fast visuomotor responses on human upper limb muscles
Uploaded: 2020-08-25T13:15:00
Description: Watch this Scientific Journal Video about An Emerging Target Paradigm to Evoke Fast Visuomotor Responses on Human Upper Limb Muscles at JoVE.com

This work is supported by a Discovery Grant to BDC from the Natural Sciences and Engineering Research Council of Canada (NSERC; RGPIN 311680) and an Operating Grant to BDC from the Canadian Institutes of Health Research (CIHR; MOP-93796). RAK was supported by an Ontario Graduate Scholarship, and ALC was supported by an NSERC CREATE grant. The experimental apparatus described in this manuscript was supported by the Canada Foundation for Innovation. Additional support came from the Canada First Research Excellence Fund (BrainsCAN).

All procedures were approved by the Health Science Research Ethics Board at the University of Western Ontario. All participants provided informed consent, were paid for their participation, and were free to withdraw&#160;from the experiment at any time.
1. Participant preparation
NOTE: A small sample of healthy, young participants was studied (3 female, 2 male; mean age: 26 years +/- 3.5). All participants were right-handed and had normal or corrected-to-normal vision...

     

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Humans have a remarkable capacity, when needed, to generate rapid, visually guided actions at latencies that approach minimal afferent and efferent conduction delays. We have previously described stimulus-locked responses (SLRs) on the upper limb as a new measure for rapid visuomotor responses6,9,10. While beneficial in providing a trial-by-trial benchmark for the first aspect of upper limb muscle recruitment influenced by the v...

When we notice a message on our cellphone, we are prompted to perform a visually guided reach to pick up our phone and read the message. Visual features such as the shape and size of the phone are transformed into motor commands allowing us to successfully reach the goal. Such visuomotor transformations may be studied in laboratory conditions, which permit a high degree of control. However, there are scenarios where response time is important, e.g., catching the phone if it were to fall. Laboratory studies of fast visuomotor behaviors often rely on displaced target paradigms where on-going movements are modified in mid-flight following some change in target position (e.g., see ref.1,2). While such online corrections can occur in &#60;150 ms3, it is difficult to ascertain the exact timing of fast visuomotor output using kinematics alone due to the low-pass filtering characteristics of the arm, and because fast visuomotor output supersedes a movement already in mid-flight. Such complications lead to uncertainty about the substrates underlying fast visuomotor responses (see ref.4 for review). Some studies suggest that subcortical structures such as the superior colliculus, rather than fronto-parietal cortical areas, may initiate online corrections5.
This uncertainty regarding the underlying neural substrates may be due, at least in part, to the lack of a reliable biomarker for the output of the fast visuomotor system. Recently, we have described a measure of fast visuomotor responses that may be generated from static postures and recorded via electromyography (EMG). Stimulus-locked responses (SLRs) are time locked bursts of EMG activity that precede voluntary movement6,7, evolving consistently ~100 ms after stimulus onset. As the name implies, SLRs are evoked by stimulus onset, persisting even if an eventual movement is withheld8 or moves in the opposite direction9. Furthermore, SLRs evoked by target displacement in a dynamic paradigm are associated with shorter latency online corrections10. Thus, SLRs provide an objective measure to systematically study the output of a fast visuomotor system involved in short latency RTs, as they may be generated from a static posture and parsed from other EMG signals unrelated to the initial phase of the fast visuomotor response.
The goal of the current study is to present a visually-guided reaching paradigm that robustly elicits SLRs. Previous studies investigating the SLR have reported less than 100% detection rates across participants, even when using more invasive intramuscular recordings6,8,9. Low detection rates and a reliance on invasive recordings limit the usefulness of SLR measures in future investigations into the fast visuomotor system in disease or across the lifespan. While some subjects may simply not express SLRs, the stimuli and behavioral paradigms used previously may not have been ideal to evoke the SLR. Past reports of SLRs have typically used paradigms wherein participants generate visually-guided reaches towards static, suddenly appearing targets6,9. However, a fast visuomotor system is the most likely needed in scenarios where one must rapidly interact with a falling or flying object, leading one&#160;to wonder if moving rather than static stimuli may better evoke SLRs. Therefore, we have adapted a moving target paradigm used to study eye movements11, and combined it with a pro/anti visually guided reaching task used to examine the SLR9. When compared to results from paradigms used previously6,8,9, it was found that SLRs in the emerging target paradigm evolved sooner, attained higher magnitudes, and were more prevalent across our participant sample. Overall, the emerging target paradigm promotes the expression of fast visuomotor responses to such a degree that objective EMG measures can be made reliably with surface recordings, potentiating study within clinical populations and across the lifespan. Further, the emerging target paradigm can be modified in many different ways, promoting more thorough investigations into the sensory, cognitive, and motor factors that promote or modify fast visuomotor responses.

<table>
	<tbody>
		<tr>
			<td>Bagnoli-8 Desktop Surface EMG System</td>
			<td>Delsys Inc.</td>
			<td></td>
			<td>Another reaching apparatus may be used</td>
		</tr>
		<tr>
			<td>Kinarm End-Point Robot</td>
			<td>Kinarm, Kingston, Ontario, Canada</td>
			<td></td>
			<td>Another reaching apparatus may be used</td>
		</tr>
		<tr>
			<td>MATLAB (version R2016a) Stateflow and Simulink applications</td>
			<td>The MathWorks, Inc., Natick, Massachusetts, United States</td>
			<td></td>
			<td></td>
		</tr>
		<tr>
			<td>PROPixx projector</td>
			<td>VPIXX Saint-Bruno, QC, Canada</td>
			<td></td>
			<td>This is a custom built addon for the Kinarm. Other displays may be used.</td>
		</tr>
		<tr>
			<td></td>
			<td></td>
			<td></td>
			<td>Resolution: 1920 x 1080. Standard viewing monitors may also be used.</td>
		</tr>
	</tbody>
</table>

an emerging target paradigm to evoke fast visuomotor responses on human upper limb muscles

To reach towards a seen object, visual information has to be transformed into motor commands. Visual information such as the object&#8217;s color, shape, and size are processed and integrated within numerous brain areas, then ultimately relayed to the motor periphery. In some instances, a reaction is needed as fast as possible. These fast visuomotor transformations, and their underlying neurological substrates, are poorly understood in humans as they have lacked a reliable biomarker. Stimulus-locked responses (SLRs) are short latency (&#60;100 ms) bursts of electromyographic (EMG) activity representing the first wave of muscle recruitment influenced by visual stimulus presentation. SLRs provide a quantifiable output of rapid visuomotor transformations, but SLRs have not been consistently observed in all subjects in past studies. Here we describe a new, behavioral paradigm featuring the sudden emergence of a moving target below an obstacle that consistently evokes robust SLRs. Human participants generated visually guided reaches toward or away from the emerging target using a robotic manipulandum while surface electrodes recorded EMG activity from the pectoralis major muscle. In comparison to previous studies that investigated SLRs using static stimuli, the SLRs evoked with this emerging target paradigm were larger, evolved earlier, and were present in all participants. Reach reaction times (RTs) were also expedited in the emerging target paradigm. This paradigm affords numerous opportunities for modification that could permit systematic study of the impact of various sensory, cognitive, and motor manipulations on fast visuomotor responses. Overall, our results demonstrate that an emerging target paradigm is capable of consistently and robustly evoking activity within a fast visuomotor system.

Stimulus locked responses (SLRs) are brief bursts of muscle activity time locked to the stimulus onset that evolve well before the larger volley of muscle recruitment associated with movement onset. The time-locked nature of the SLR produced a &#8216;banding&#8217; of muscle activity visible at ~100 ms when viewing all trials sorted for reaction time (RT) (Figure 1a, highlighted by grey boxes). As shown in Figure 1a, SLRs was dependent on target location, with S...

Watch this Scientific Journal Video about An Emerging Target Paradigm to Evoke Fast Visuomotor Responses on Human Upper Limb Muscles at JoVE.com

An Emerging Target Paradigm to Evoke Fast Visuomotor Responses on Human Upper Limb Muscles

Presented here is a behavioral paradigm that elicits robust fast visuomotor responses on human upper limb muscles during visually guided reaches.

To reach towards a seen object, visual information has to be transformed into motor commands. Visual information such as the object&#8217;s color, shape, ...

We are interested in how the brain can rapidly translate visual input into motor output. And here, we describe the emerging target paradigm, which elicits quantifiable and reliable fast visuomotor responses. The fast visuomotor responses listed by the paradigm include stimulus-locked responses, which are short bursts of muscle activity tied to visual stimulus onset.Having a paradigm that reliably elicits fast visuomotor responses potentiates the study of the underlying neural mechanisms across the lifespan and in neurological disorders like Parkinson's disease. Many aspects of the emerging target paradigm could be modified to better understand the sensory, cognitive, and motor factors which influence the fast visuomotor system. Begin by applying electromyography or EMG sensors to the targeted upper limb muscle involved in the reaching movement being studied.Visualize the target muscle by requesting an action known to recruit the muscle of interest. For the clavicular head of the pectoralis major muscle, ask the participant to relax their elbows at their sides and push their palms together. If it is difficult to visualize the target muscle, palpate the area of interest while having the participant repeatedly perform the requested action.Target areas with notable changes in the muscle for electrode placement. Use alcohol swabs to clean the skin areas where electrodes will be located and apply adhesives and electrode gel to the surface sensors. Ask the participant to perform the action associated with the muscle recruitment again and adhere sensors over the muscle belly, positioning them to lie in parallel with the direction of the fibers of the targeted muscle.Place the ground electrode on the clavicle contralateral to the reaching arm, then secure sensors and ground electrodes to the surrounding skin with medical tape. Turn on the EMG system to allow for EMG collection throughout the experiment. Check the quality of the EMG signal with a desktop monitor or oscilloscope connected to the system.Have the participant perform a reaching movement into or opposite from the preferred direction of the muscle of interest and ensure that the EMG activity increases or decreases respectively. Next, set up the participant in a robotic reaching apparatus that allows reaching movements in a horizontal plane and the application of force to the manipulandum. Seat the participant in the experimental chair, maximizing their comfort to minimize changes of posture throughout the experiment.Click start on the associated software which initiates the first trial and force generated by the robotic reaching apparatus applied to the participant's upper limb. Verbally instruct the participant to start the first trial by bringing the real-time cursor or RTC into the start position for a duration of one to 1.5 seconds. The occluder changes color to instruct the subject that the upcoming trial requires a pro or anti-reach.Determine if the participant is able to generate a visually-guided reach depending on the color of the occluder. When the occluder is green, the participant intercepts the moving target with the RTC. When the occluder is red, the participant moves the RTC away from the target.Ensure that the moving target, which was stationary and visible to the participant at the top of the inverted Y, begins moving towards the participant along the path of the inverted Y.When the moving target moves behind the occluder, it should move at a constant speed of 30 centimeters per second along the y-axis and should be invisible to the participant. During this interval, the participant should maintain the hand position at the imagined start position. Once the moving target reaches half the length of the occluder, it bifurcates along one of the inverted Y outputs with an additional X velocity component.The target vanishes for a constant delay of approximately half a second, with the delay depending on the size of the occluder and the speed of the target. When the moving target reaches the edge of the occluder, make sure that the software keeps it invisible until the full target has emerged and only then presents it to the participant. The target should be presented to a randomized side at one of the inverted Y paths while the participant's hand remains at the starting position.The exact time of target emergence must be known to ensure accurate measurement of fast visuomotor responses. Here, we present another visual stimulus, which is not seen by the participant, to a photodiode located in the corner of the screen at the exact time of target emergence. This photodiode provides an analog signal for alignment of muscle activity and reaction times.Depending on the participant's reaching behavior, this software provides feedback as text written on the occluder during the inter-trial interval. The feedback says hit for correct interception, wrong way for incorrect direction of reach, or miss for neither correct nor incorrect responses detected during the inter-trial interval. The moving target and the starting position reappear at their respective original locations 200 milliseconds after the participant's reach behavior is completed.Start the next trial when the participant brings the RTC to the starting position. Minimize the participant's movement between each block to ensure consistency of recordings. After verbal confirmation that the participant is ready to begin the next block, initiate the next block and continue to monitor participant performance and EMG output.Stimulus-locked responses or SLRs depended on target location, with SLRs on the right pectoralis major consisting of an increase or decrease in muscle recruitment following leftward or rightward target presentation respectively. To detect SLRs, separate time series receiver operating characteristic analyses were performed on trials with earlier or later than average reaction times. This analysis indicated whether electromyography onset was invariant to stimulus or movement onset, which was determined by the slope of the line connecting early and late discrimination times plotted as a function of reaction time.Data from two subjects reaching toward a stationary object or moving target is shown here. Participant one does not exhibit an SLR in the static paradigm, but a clear SLR can be seen in the emerging target paradigm. The SLR was also apparent in the mean electromyography traces for participant one in the emerging target paradigm.While participant two exhibited an SLR in both the static and emerging target paradigms, the magnitude of the SLR was much greater in the emerging target paradigm. On average, SLR magnitude was considerably larger in the emerging target versus the static paradigm. In contrast, the latency of detected SLRs did not differ between the two paradigms.SLRs were detected in all five participants in the emerging target paradigm, but only in three participants in a paradigm with static targets. SLR magnitudes in the anti-reach condition were muted compared to that in the pro-reach condition. The paradigm could be varied to better understand the sensory, cognitive, or motor factors that influence fast visuomotor responses.Future experiments could vary target speed, alter the time behind the occluder, or require participants to choose which hand to move. We've started to use reliable responses elicited by the emerging target paradigm to study the fast visuomotor system in elderly participants and in patients with Parkinson's disease.

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