scholarly journals Short-latency afferent inhibition and somato-sensory evoked potentials during the migraine cycle: surrogate markers of a cycling cholinergic thalamo-cortical drive?

2020 ◽  
Author(s):  
Gianluca Coppola ◽  
Davide Di Lenola ◽  
Chiara Abagnale ◽  
Fabio Ferrandes ◽  
Gabriele Sebastianelli ◽  
...  

Abstract Background: Short-latency afferent inhibition (SAI) consists of motor cortex inhibition induced by sensory afferents and depends on the excitatory effect of cholinergic thalamocortical projections on inhibitory GABAergic cortical networks. Given the electrophysiological evidence for thalamo-cortical dysrhythmia in migraine, we studied SAI in migraineurs during and between attacks and searched for correlations with somatosensory habituation, thalamocortical activation, and clinical features.Methods: SAI was obtained by conditioning the transcranial magnetic stimulation-induced motor evoked potential (MEP) with an electric stimulus on the median nerve at the wrist with random stimulus intervals corresponding to the latency of individual somatosensory evoked potentials (SSEP) N20 plus 2, 4, 6, or 8 ms. We recruited 30 migraine without aura patients, 16 between (MO), 14 during an attack (MI), and 16 healthy volunteers (HV). We calculated the slope of the linear regression between the unconditioned MEP amplitude and the 4-conditioned MEPs as a measure of SAI. We also measured SSEP amplitude habituation, and high-frequency oscillations (HFO) as an index of thalamo-cortical activation.Results: Compared to HV, SAI, SSEP habituation and early SSEP HFOs were significantly reduced in MO patients between attacks, but enhanced during an attack. There was a positive correlation between degree of SAI and amplitude of early HFOs in HV, but not in MO or MI. When the two patient groups were pooled, both the MEP SAI slope and the SSEP habituation slope correlated positively with the number of days elapsed since the last migraine attack.Conclusions: The migraine cycle-dependent variations of SAI and SSEP HFOs are further evidence that facilitatory thalamocortical activation (of GABAergic networks in the motor cortex for SAI), likely to be cholinergic, is reduced in migraine at a distance from an attack, but increased ictally.

2020 ◽  
Author(s):  
Gianluca Coppola ◽  
Davide Di Lenola ◽  
Chiara Abagnale ◽  
Fabio Ferrandes ◽  
Gabriele Sebastianelli ◽  
...  

Abstract Background: Short-latency afferent inhibition (SAI) consists of motor cortex inhibition induced by sensory afferents and depends on the excitatory effect of cholinergic thalamocortical projections on inhibitory GABAergic cortical networks. Given the electrophysiological evidence for thalamo-cortical dysrhythmia in migraine, we studied SAI in migraineurs during and between attacks and searched for correlations with somatosensory habituation, thalamocortical activation, and clinical features. Methods: SAI was obtained by conditioning the transcranial magnetic stimulation-induced motor evoked potential (MEP) with an electric stimulus on the median nerve at the wrist with random stimulus intervals corresponding to the latency of individual somatosensory evoked potentials (SSEP) N20 plus 2, 4, 6, or 8 ms. We recruited 30 migraine without aura patients, 16 between (MO), 14 during an attack (MI), and 16 healthy volunteers (HV). We calculated the slope of the linear regression between the unconditioned MEP amplitude and the 4-conditioned MEPs as a measure of SAI. We also measured SSEP amplitude habituation, and high-frequency oscillations (HFO) as an index of thalamo-cortical activation. Results: Compared to HV, SAI, SSEP habituation and early SSEP HFOs were significantly reduced in MO patients between attacks, but enhanced during an attack. There was a positive correlation between degree of SAI and amplitude of early HFOs in HV, but not in MO or MI. Conclusions: The migraine cycle-dependent variations of SAI and SSEP HFOs are further evidence that facilitatory thalamocortical activation (of GABAergic networks in the motor cortex for SAI), likely to be cholinergic, is reduced in migraine between attacks, but increased ictally.


2020 ◽  
Vol 123 (3) ◽  
pp. 1052-1062 ◽  
Author(s):  
Jasmine L. Mirdamadi ◽  
Hannah J. Block

Trial-and-error motor adaptation has been linked to somatosensory plasticity and shifts in proprioception (limb position sense). The role of sensory processing in motor skill learning is less understood. Unlike adaptation, skill learning involves the acquisition of new movement patterns in the absence of perturbation, with performance limited by the speed-accuracy trade-off. We investigated somatosensory changes during motor skill learning at the behavioral and neurophysiological levels. Twenty-eight healthy young adults practiced a maze-tracing task, guiding a robotic manipulandum through an irregular two-dimensional track featuring several abrupt turns. Practice occurred on days 1 and 2. Skill was assessed before practice on day 1 and again on day 3, with learning indicated by a shift in the speed-accuracy function between these assessments. Proprioceptive function was quantified with a passive two-alternative forced-choice task. In a subset of 15 participants, we measured short-latency afferent inhibition (SAI) to index somatosensory projections to motor cortex. We found that motor practice enhanced the speed-accuracy skill function ( F4,108 = 32.15, P < 0.001) and was associated with improved proprioceptive sensitivity at retention ( t22 = 24.75, P = 0.0031). Furthermore, SAI increased after training ( F1,14 = 5.41, P = 0.036). Interestingly, individuals with larger increases in SAI, reflecting enhanced somatosensory afference to motor cortex, demonstrated larger improvements in motor skill learning. These findings suggest that SAI may be an important functional mechanism for some aspect of motor skill learning. Further research is needed to test what parameters (task complexity, practice time, etc.) are specifically linked to somatosensory function. NEW & NOTEWORTHY Somatosensory processing has been implicated in motor adaptation, where performance recovers from a perturbation such as a force field. We investigated somatosensory function during motor skill learning, where a new motor pattern is acquired in the absence of perturbation. After skill practice, we found changes in proprioception and short-latency afferent inhibition (SAI), signifying somatosensory change at both the behavioral and neurophysiological levels. SAI may be an important functional mechanism by which individuals learn motor skills.


2016 ◽  
Vol 116 (2) ◽  
pp. 637-644 ◽  
Author(s):  
Aaron Z. Bailey ◽  
Michael J. Asmussen ◽  
Aimee J. Nelson

Short-latency afferent inhibition (SAI) is characterized by the suppression of the transcranial magnetic stimulation motor evoked potential (MEP) by the cortical arrival of a somatosensory afferent volley. It remains unknown whether the magnitude of SAI reflects changes in the sensory afferent volley, similar to that observed for somatosensory evoked potentials (SEPs). The present study investigated stimulus-response relationships between sensory nerve action potentials (SNAPs), SAI, and SEPs and their interrelatedness. Experiment 1 ( n = 23, age 23 ± 1.5 yr) investigated the stimulus-response profile for SEPs and SAI in the flexor carpi radialis muscle after stimulation of the mixed median nerve at the wrist using ∼25%, 50%, 75%, and 100% of the maximum SNAP and at 1.2× and 2.4× motor threshold (the latter equated to 100% of the maximum SNAP). Experiment 2 ( n = 20, age 23.1 ± 2 yr) probed SEPs and SAI stimulus-response relationships after stimulation of the cutaneous digital nerve at ∼25%, 50%, 75%, and 100% of the maximum SNAP recorded at the elbow. Results indicate that, for both nerve types, SAI magnitude is dependent on the volume of the sensory afferent volley and ceases to increase once all afferent fibers within the nerve are recruited. Furthermore, for both nerve types, the magnitudes of SAI and SEPs are related such that an increase in excitation within somatosensory cortex is associated with an increase in the magnitude of afferent-induced MEP inhibition.


2012 ◽  
Vol 108 (1) ◽  
pp. 314-323 ◽  
Author(s):  
Florinda Ferreri ◽  
David Ponzo ◽  
Taina Hukkanen ◽  
Esa Mervaala ◽  
Mervi Könönen ◽  
...  

When linking in time electrical stimulation of the peripheral nerve with transcranial magnetic stimulation (TMS), the excitability of the motor cortex can be modulated to evoke clear inhibition, as reflected by the amplitude decrement in the motor-evoked potentials (MEPs). This specific property, designated short-latency afferent inhibition (SAI), occurs when the nerve–TMS interstimulus interval (ISI) is approximately 25 ms and is considered to be a corticothalamic phenomenon. The aim of the present study was to use the electroencephalographic (EEG) responses to navigated-TMS coregistration to better characterize the neuronal circuits underlying SAI. The present experimental set included magnetic resonance imaging (MRI)–navigated TMS and 60-channel TMS-compatible EEG devices. TMS-evoked EEG responses and MEPs were analyzed in eight healthy volunteers; ISIs between median nerve and cortical stimulation were determined relative to the latency of the individual N20 component of the somatosensory-evoked potential (SEP) obtained after stimulation of the median nerve. ISIs from the latency of the N20 plus 3 ms and N20 plus 10 ms were investigated. In all experimental conditions, TMS-evoked EEG responses were characterized by a sequence of negative deflections peaking at approximately 7, 44, and 100 ms alternating with positive peaks at approximately 30, 60, and 180 ms post-TMS. Moreover, ISI N20+3 ms modulated both EEG-evoked activity and MEPs. In particular, it inhibited MEP amplitudes, attenuated cortical P60 and N100 responses, and induced motor cortex beta rhythm selective decrement of phase locking. The findings of the present experiment suggest the cortical origin of SAI that could result from the cortico–cortical activation of GABAergic-mediated inhibition onto the corticospinal neurons modulated by cholinergic activation able to reducing intralaminar inhibition and promoting intracolumnar inhibition.


Neurology ◽  
2006 ◽  
Vol 66 (7) ◽  
pp. 1111-1113 ◽  
Author(s):  
V. Di Lazzaro ◽  
F. Pilato ◽  
M. Dileone ◽  
E. Saturno ◽  
A. Oliviero ◽  
...  

The test of short latency afferent inhibition (SAI) of the motor cortex is helpful in demonstrating dysfunction of central cholinergic circuits in Alzheimer disease (AD). The authors evaluated SAI in 20 patients with frontotemporal dementia (FTD) and compared data with those from 20 patients with AD and 20 controls. SAI was normal in FTD, whereas it was reduced in AD. SAI may represent an additional tool to discriminate FTD from AD.


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