A subcortical origin for rapid, target-oriented corticospinal excitability modulation during visually guided reaching

Divakar, Rechu; Loeb, Gerald E.; Wallis, Guy; Carroll, Timothy J.

doi:10.1101/2022.12.13.520229

Cited by 3 publications

(6 citation statements)

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“…Follow up pairwise comparisons showed that corticospinal excitability at 80 ms was influenced by the location of the target in both pro-( P = 0.005, Figure 7A ) and anti-reach conditions ( P = 0.007, Figure 7B ). This is consistent with the early target-oriented excitability changes observed earlier (Divakar et al, 2022), confirming our finding that the visual information has rapid access to the corticospinal tract as early as 80 ms. In that paper, we saw that the target-related MEP changes at 80 ms were immediately followed by the movement-related changes at 90-100 ms. By contrast, here we saw a significant temporal gap between the early target-related and late movement-related excitability changes.…”

Section: Resultssupporting

confidence: 93%

“…In experiment two, neither the MEP nor the background EMG was influenced by goal-directed activity in the early stages of reaching ( Figure 7 ). This confirms that the early excitability changes that we reported previously (Divakar et al, 2022) were due at least in part to the express visuomotor response and not due solely to an overlap with the early voluntary response. The results from the two experiments in the current study were also consistent, in that both MEPs and background EMG prior to 140 ms appeared to show an alternating pattern in both pro- and anti-reach conditions, with clear target-oriented MEP modulation at 80 ms ( Figure 7 ).…”

Section: Discussionsupporting

confidence: 91%

“…The general setup used in the study ( Figure 1A ) has been described previously (Divakar et al, 2022). Briefly, in both experiments 1 and 2, we used an emerging target paradigm ( Figure 1B ) that has been shown to promote short latency muscle responses (Kozak et al, 2019; Contemori et al, 2020).…”

Section: Methodsmentioning

confidence: 99%

“…To calculate the underlying muscle activity or background EMG, in the absence of TMS, we looked at the muscle activity in the no stimulation trials ( noStim trials) that were intermixed with the stimulation trials. As in detailed in Divakar et al (2022), we measured the average of the rectified EMG in the noStim trials from the same time window that was used to calculate the MEP in the stimulation trials. This time window was called the ‘measurement window’.…”

Section: Methodsmentioning

confidence: 99%

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A complex reach direction rule that delays reaction time causes alternating excitation and inhibition in express muscle responses and corticospinal excitability

Divakar

Loeb

Wallis

et al. 2022

Preprint

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The dynamics of muscle activation during fast visually guided reaching are suggestive of two neural control signals; an early signal that acts at 'express' latencies in response to the visual stimulus, and a longer latency signal that executes a strategic reach plan. Here we developed a task designed to temporally isolate the express visuomotor response from the longer latency muscle response, and to characterize the time course of corticospinal excitability changes in the express response time window when the late voluntary response is delayed. We tested this by measuring electromyograms (EMG) and changes in Motor Evoked Potential (MEP) amplitudes following Transcranial Magnetic Stimulation (TMS) of the motor cortex, as participants reached either towards or away from visual targets. Crucially, the information about the task rule was provided by the luminance of the target itself, and so was unknown to the subject until the instant of target presentation. This feature delayed reaction times, likely because additional (presumably cortical) processing was required to interpret and apply the rule before formation of a goal directed reach plan. The earliest EMG responses to target presentation occurred with a 70-105 ms time window, and were oriented to bring the hand toward the location of the target. However, there was also a slightly later response that was also time-locked to target appearance in a 105-140 ms time window. This second response was 'reciprocal' to the first, such that it was oriented to take the hand in the direction opposite from the target. In some participants, additional oscillating cycles were apparent after the first two target-related responses. These multiphasic express visuomotor responses were nearly identical in both pro- and anti-reach conditions. These muscle activity responses were generally reflected in the temporal pattern of corticospinal excitability modulations in experiment two. Indeed, the MEP and background EMG responses showed an alternating pattern similar to that in experiment one, although the effect was clearer in the anti-reach than the pro-reach condition. Overall, the data show that the express and voluntary responses are indeed distinct neural control signals, which supports the hypothesis that at least two separate neural pathways (one slow and one fast) contribute to the control of visually guided reaching. The properties of the fast pathway are consistent with a tecto-reticulospinal pathway, while those of the slow pathway are consistent with a transcortical loop.

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Section: Resultssupporting

confidence: 93%

Section: Discussionsupporting

confidence: 91%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

A complex reach direction rule that delays reaction time causes alternating excitation and inhibition in express muscle responses and corticospinal excitability

Divakar

Loeb

Wallis

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Reach-related neurons in the dSC display short-latency visual responses (Werner et al, 1997a(Werner et al, , 1997b and correlate with upper limb muscle activity (Werner et al, 1997a;Stuphorn et al, 1999), although the properties of visual responses in reachrelated neurons have not been systematically investigated. Our speculation of a subcortical route initiating visually-guided reaches to a punctate target is consistent with recent stimulation results in humans (Divakar et al, 2022), and parallels a growing appreciation for the role of subcortical pathways in manual following responses to whole-field motion (Saijo et al, 2005) or flashes (Nakajima et al, 2021).…”

Section: Implications Of Our Resultssupporting

confidence: 89%

Done in 65 ms: Express visuomotor responses in upper limb muscles in Rhesus Macaques

Cecala

Kozak

Pruszynski

2023

Preprint

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How rapidly can the brain transform vision into action? Work in humans has established that the transformation for visually-guided reaching can be remarkably rapid, with the first phase of upper limb muscle recruitment, theexpress visuomotor response, beginning within less than 100 ms of visual target presentation. Such short-latency responses limit the opportunities for extensive cortical processing, leading to the hypothesis that they are generated via the subcortical tectoreticulospinal pathway. Here, we examine if non-human primates (NHPs) exhibit express visuomotor responses. Two male macaques made visually-guided reaches in a behavioral paradigm known to elicit express visuomotor responses in humans, while we acquired intramuscular recordings from the deltoid muscle. Across several variants of this paradigm, express visuomotor responses began within 65 ms (range 48–91 ms) of target presentation. Although the timing of the express visuomotor response did not co-vary with reaction time, larger express visuomotor responses tended to precede shorter latency reaches. Finally, the magnitude of the express visuomotor response was muted on trials where NHPs withheld a reach to one stimulus in order to move to a stimulus appearing 34 ms later in the opposite direction. Overall, the response properties and contextual control of express visuomotor responses in NHPs resemble those in humans. Our results establish a new benchmark for visuomotor transformations underlying visually-guided reaches, setting the stage for experiments that can directly test the comparative role of cortical and subcortical areas in reaching when time is of the essence.Significance statementExpress visuomotor responses in upper limb muscles are brief periods of recruitment preceding visually-guided reaches. Such responses begin ∼90 ms after visual target presentation in humans, and potentially arise from signaling along the tecto-reticulo-spinal pathway. Here, we show that express visuomotor responses in macaques upper limb muscles resemble those in humans, excepting that they evolve ∼65 ms after target onset, consistent with shorter responses latencies in macaques versus humans. Our results clock the completion of the visuomotor transformation for rapid reaching, and set the stage for experiments to directly test the underlying substrates.

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Done in 65 ms: Express Visuomotor Responses in Upper Limb Muscles in Rhesus Macaques

Cecala

Kozak

Pruszynski

2023

eNeuro

Self Cite

View full text Add to dashboard Cite

How rapidly can the brain transform vision into action? Work in humans has established that the transformation for visually-guided reaching can be remarkably rapid, with the first phase of upper limb muscle recruitment, theexpress visuomotor response, beginning within less than 100 ms of visual target presentation. Such short-latency responses limit the opportunities for extensive cortical processing, leading to the hypothesis that they are generated via the subcortical tectoreticulospinal pathway. Here, we examine if non-human primates (NHPs) exhibit express visuomotor responses. Two male macaques made visually-guided reaches in a behavioral paradigm known to elicit express visuomotor responses in humans, while we acquired intramuscular recordings from the deltoid muscle. Across several variants of this paradigm, express visuomotor responses began within 65 ms (range 48–91 ms) of target presentation. Although the timing of the express visuomotor response did not co-vary with reaction time, larger express visuomotor responses tended to precede shorter latency reaches. Further, we observed that the magnitude of the express visuomotor response could be muted by contextual context, although this effect was quite variable. Overall, the response properties in NHPs resemble those in humans. Our results establish a new benchmark for visuomotor transformations underlying visually-guided reaches, setting the stage for experiments that can directly compare the role of cortical and subcortical areas in reaching when time is of the essence.Significance statementExpress visuomotor responses in upper limb muscles are brief periods of recruitment preceding visually-guided reaches. Such responses begin ∼90 ms after visual target presentation in humans, and potentially arise from signaling along the tecto-reticulo-spinal pathway. Here, we show that express visuomotor responses in macaques upper limb muscles resemble those in humans, excepting that they evolve ∼65 ms after target onset, consistent with shorter responses latencies in macaques versus humans. Our results clock the completion of the visuomotor transformation for rapid reaching, and set the stage for experiments to directly test the underlying substrates.

show abstract

A subcortical origin for rapid, target-oriented corticospinal excitability modulation during visually guided reaching

Cited by 3 publications

References 84 publications

A complex reach direction rule that delays reaction time causes alternating excitation and inhibition in express muscle responses and corticospinal excitability

A complex reach direction rule that delays reaction time causes alternating excitation and inhibition in express muscle responses and corticospinal excitability

Done in 65 ms: Express visuomotor responses in upper limb muscles in Rhesus Macaques

Done in 65 ms: Express Visuomotor Responses in Upper Limb Muscles in Rhesus Macaques

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