Relationship between high-frequency activity in the cortical sensory and the motor hand areas, and their myelin content

Tomasevic, L.; Siebner, Hartwig R.; Thielscher, Axel; Manganelli, Fiore; Pontillo, Giuseppe; Dubbioso, Raffaele

doi:10.1016/j.brs.2022.04.018

Cited by 7 publications

(9 citation statements)

References 79 publications

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“…For example, for somatosensory evoked potentials (SSEPs) elicited by electrical stimulation of the median nerve, the slower negative wave observed at around 20ms after stimulation (N20) is combined with high frequency oscillations (>600Hz) generated in the same cortical region [23,24]. Furthermore, results from our lab have confirmed and elaborated this notion by linking high-frequency somatosensory responses to high-frequency changes in intracortical excitability of M1 HAND probed with a short-latency intracortical facilitation (SICF) paired-pulse protocol [25]. Furthermore, comparable cortical responses can be recorded from the motor cortex following deep electrical stimulation of the subthalamic nucleus likely via antidromic activation of the hyperdirect pathway [26].…”

Section: Discussionmentioning

confidence: 87%

Transcranial magnetic stimulation of primary motor cortex elicits a site-specific immediate transcranial evoked potential

Beck,

Christiansen,

Madsen

et al. 2023

Preprint

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Background Transcranial evoked potentials (TEPs) measured via electroencephalography (EEG) are widely used to study the cortical responses to transcranial magnetic stimulation (TMS). Immediate transcranial evoked potentials (i-TEPs) have been obscured by pulse and muscular artifacts. Thus, the TEP peaks that are commonly reported have latencies that are too long to be caused by direct excitation of cortical neurons. Methods In 14 healthy individuals, we recorded i-TEPs evoked by a single biphasic TMS pulse targeting the primary motor hand area (M1_HAND) or parietal or midline control sites. Sampling EEG at 50 kHz enabled us to reduce the duration of the TMS pulse artifact to a few milliseconds, while minor adjustments of the TMS coil tilt or position enabled us to avoid cranial muscular twitches during the experiment. Results We observed an early positive EEG deflection starting after approx. 2 ms followed by a series of superimposed peaks with an inter-peak interval of ~1.1-1.4 ms in multiple electrodes overlying the stimulated sensorimotor region. This multi-peak i-TEP response was only evoked by TMS of the M1_HAND region and was modified by changes in stimulation intensity and current direction. Discussion Single-pulse TMS of the M1_HAND evokes an immediate local multi-peak response at the cortical site of stimulation. Our results suggest that the observed i-TEP patterns are genuine cortical responses evoked by TMS caused by synchronized excitation of pyramidal neurons in the targeted precentral cortex. This notion needs to be corroborated in future studies, including further investigations into the potential contribution of instrumental or physiological artifacts.

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Section: Discussionmentioning

confidence: 87%

Transcranial magnetic stimulation of primary motor cortex elicits a site-specific immediate transcranial evoked potential

Beck,

Christiansen,

Madsen

et al. 2023

Preprint

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“…In conclusion, RAPNs in zebra finches exhibit many fundamental molecular and functional similarities to primate Betz cells, that may be involved is fine digit movements (Tomasevic et al, 2022). In combination with their well-defined role in singing behaviors, this study identifies RAPNs as a novel and more accessible model for studying the properties of Betz-like pyramidal neurons that offer the temporal precision required to control complex learned motor behaviors.…”

Section: Discussionmentioning

confidence: 99%

“…Remarkably, Betz cells are absent in rodent M1 cortex (Lacey et al, 2014; Soares et al, 2017). Studies of Betz-like cells have thus been hindered by species accessibility and because these specialized cells are interspersed with other smaller L5PNs in M1 cortex (Clustered in cotrical areas for fine digit control in humans; (Rivara, Sherwood, Bouras, & Hof, 2003; Tomasevic et al, 2022)).…”

Section: Introductionmentioning

confidence: 99%

Cortical Betz cells analogue in songbirds utilizes Kv3.1 to generate ultranarrow spikes

Zemel

Nevue

Tavares

et al. 2022

Preprint

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Complex motor skills in vertebrates require specialized upper motor neurons with precise action potential (AP) firing. To examine how diverse populations of upper motor neurons subserve distinct functions and the specific repertoire of ion channels involved, we conducted a thorough study of the excitability of upper motor neurons controlling somatic motor function in the zebra finch. We found that robustus arcopallialis projection neurons (RAPNs), key command neurons for song production, exhibit ultranarrow spikes and higher firing rates compared to neurons controlling non-vocal somatic motor functions (AId neurons). This striking difference was primarily due to the expression of a high threshold, fast-activating voltage-gated K+ channel, Kv3.1 (KCNC1). RAPN properties thus mirror those of the sparse, specialized Betz cells in the motor cortex of humans and other primates, which also fire ultranarrow spikes enabled by Kv3.1 expression. These large layer 5 pyramidal neurons are involved in fine digit control and are notably absent in rodents. Our study thus provides evidence that songbird RAPNs and primate Betz cells have convergently evolved the use of Kv3.1 to ensure precise, rapid AP firing required for fast and complex motor skills.

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“…Second, we measured only SEP and PPI to evaluate S1 excitability. To clarify the change in neural balance between excitation and inhibition in the S1 in greater detail, it would be preferable to investigate other biomarkers of inhibitory function such as early and late components of SEP high-frequency oscillation (e- and l-HFO) ( Erro et al, 2018 ; Dubbioso et al, 2022 ; Tomasevic et al, 2022 ), which reflect the activity of thalamocortical fibers directed to areas 3b and 1 within S1 and intracortical inhibition in S1, putatively a result of local GABAergic interneurons. Third, the effects of the present interventions on several somatosensory functions remain unclear.…”

Section: Discussionmentioning

confidence: 99%

Effect of whole-hand water flow stimulation on the neural balance between excitation and inhibition in the primary somatosensory cortex

Cong

Sato²,

Ikarashi³

et al. 2022

Front. Hum. Neurosci.

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Sustained peripheral somatosensory stimulations, such as high-frequency repetitive somatosensory stimulation (HF-RSS) and vibrated stimulation, are effective in altering the balance between excitation and inhibition in the somatosensory cortex (S1) and motor cortex (M1). A recent study reported that whole-hand water flow (WF) stimulation induced neural disinhibition in the M1. Based on previous results, we hypothesized that whole-hand WF stimulation would lead to neural disinhibition in the S1 because there is a strong neural connection between M1 and S1 and aimed to examine whether whole-hand WF stimulation would change the neural balance between excitation and inhibition in the S1. Nineteen healthy volunteers were studied by measuring excitation and inhibition in the S1 before and after each of the four 15-min interventions. The excitation and inhibition in the S1 were assessed using somatosensory evoked potentials (SEPs) and paired-pulse inhibition (PPI) induced by single- and paired-pulse stimulations, respectively. The four interventions were as follows: control, whole-hand water immersion, whole-hand WF, and HF-RSS. The results showed no significant changes in SEPs and PPI following any intervention. However, changes in PPI with an interstimulus interval (ISI) of 30 ms were significantly correlated with the baseline value before whole-hand WF. Thus, the present findings indicated that the whole-hand WF stimulation had a greater decreased neural inhibition in participants with higher neural inhibition in the S1 at baseline. Considering previous results on M1, the present results possibly show that S1 has lower plasticity than M1 and that the duration (15 min) of each intervention may not have been enough to alter the balance of excitation and inhibition in the S1.

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Relationship between high-frequency activity in the cortical sensory and the motor hand areas, and their myelin content

Cited by 7 publications

References 79 publications

Transcranial magnetic stimulation of primary motor cortex elicits a site-specific immediate transcranial evoked potential

Transcranial magnetic stimulation of primary motor cortex elicits a site-specific immediate transcranial evoked potential

Cortical Betz cells analogue in songbirds utilizes Kv3.1 to generate ultranarrow spikes

Effect of whole-hand water flow stimulation on the neural balance between excitation and inhibition in the primary somatosensory cortex

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