Visual information increases the indirect corticospinal excitation via cervical interneurons in humans

Nakajima, Toshikatsu; Ohtsuka, Hiroyuki; Irie, Shun; Suzuki, Shinya; Ariyasu, Ryohei; Komiyama, Tomoyoshi; Ohki, Yukari

doi:10.1152/jn.00425.2020

Cited by 8 publications

(7 citation statements)

References 65 publications

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“…The timing of corticospinal excitability effects induced by visual stimulation observed here is broadly consistent with previous reports by Nakajima et al 2021 found that a bright visual flash enhanced the single TMS/TES-induced MEPs in the biceps brachii muscle from 60 ms, when the arm was stationary and under tonic contraction (Nakajima et al, 2021). Suzuki et al 2021 used a target jump paradigm during an ongoing reach and found modulation in MEPs from 70 ms in the biceps and triceps muscles (involved in making the corrective reach towards the target) that depended on the direction of the target jump (Suzuki et al, 2021).…”

Section: Discussionsupporting

confidence: 92%

“…The timing of corticospinal excitability effects induced by visual stimulation observed here is broadly consistent with previous reports by Nakajima et al 2021 and Suzuki et al 2021. Nakajima et al 2021 found that a bright visual flash enhanced the single TMS/TES-induced MEPs in the biceps brachii muscle from 60 ms, when the arm was stationary and under tonic contraction (Nakajima et al, 2021).…”

Section: Discussionsupporting

confidence: 92%

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

Divakar

Loeb

Wallis

et al. 2022

Preprint

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During visually guided reaching, proximal limb muscles can be activated within 80 ms of target appearance. Such 'express' visuomotor responses are temporally aligned with target appearance rather than movement onset, and invariably tuned towards the direction of the visual target regardless of the instructed reach direction. These features prompt the hypothesis that express visuomotor responses are driven by a subcortical pathway. We tested this by measuring the changes in Motor Evoked Potentials (MEPs) following Transcranial Magnetic Stimulation (TMS) or Transcranial Electrical Stimulation (TES) of the motor cortex as participants reached either towards or away from visual targets. We found that 70-80 ms after target presentation, MEPs in primary shoulder flexor muscle (pectoralis major) were oriented towards the target direction regardless of whether the participant subsequently reached towards or away from the target. Similar target-oriented MEP modulations were seen in posterior deltoid and biceps brachii, whereas MEPs in a finger muscle were affected neither by target nor reach direction. Critically, there were no significant differences in modulation of responses to TMS and TES across all reaching conditions, which suggests that the target-oriented modulation occurs downstream of the motor cortex output neurons. Combined, our results show that rapid target-oriented corticospinal excitability changes are tuned to the location of the visual target and at least partly driven by a subcortical pathway. A prime candidate for such subcortical modulation involves the superior colliculus and reticular formation.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 92%

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

Divakar

Loeb

Wallis

et al. 2022

Preprint

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“…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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“…Very rapid on-line corrections can also be shared across the upper and lower limbs, presumably via subcortical pathways (45). Further, by combining transcranial brain stimulation and electrical stimulation of the median nerve, Nakajima, Suzuki and colleagues (46,47) proposed that rapid limb responses to changing visual inputs arose from integration within cervical interneurons of corticospinal inputs with visual information rapidly relayed along a subcortical tectoreticulospinal pathways. Whether cervical interneurons are involved in the generation of express arm responses, perhaps in conjunction with the reticular formation, remains to be determined but this seems likely given the broad convergence between descending motor pathways (42).…”

Section: Neural Substrates For the Express Arm Responsementioning

confidence: 99%

Express arm responses appear bilaterally on upper-limb muscles in an arm choice reaching task

Kearsley

Cecala

Kozak

2022

Journal of Neurophysiology

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When required, humans can generate very short latency reaches towards visual targets, like catching a falling cellphone. During such rapid reaches, express arm responses are the first wave of upper limb muscle recruitment, occurring ~80-100 ms after target appearance. There is accumulating evidence that express arm responses arise from signaling along the tecto-reticulo-spinal tract, but the involvement of the reticulo-spinal tract has not been well-studied. Since the reticulospinal tract projects bilaterally, we studied whether express arm responses would be generated bilaterally. Human participants (n = 14; 7 female) performed visually guided reaches in a modified emerging target paradigm where either arm could intercept the target. We recorded electromyographic activity bilaterally from the pectoralis major muscle. Our analysis focused on target locations where participants reached with the right arm on some trials, and the left arm on others. In support of the involvement of the reticulospinal tract, express arm responses persisted bilaterally regardless of which arm reached to the target. The latency and magnitude of the express arm response did not depend on whether the arm was chosen to reach or not. However, on the reaching arm, the magnitude of the express arm response was correlated to the level of anticipatory activity. The bilateral generation of express arm responses supports the involvement of the reticulo-spinal tract. We surmise that the correlation between anticipatory activity and the magnitude of express arm responses on the reaching arm arises from convergence of cortically-derived signals with a parallel subcortical pathway mediating the express arm response.

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Visual information increases the indirect corticospinal excitation via cervical interneurons in humans

Cited by 8 publications

References 65 publications

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

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

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

Express arm responses appear bilaterally on upper-limb muscles in an arm choice reaching task

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