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Cross-Streams Through the Ventral Posteromedial Thalamic Nucleus to Convey Vibrissal Information

ABSTRACT: Whisker detection is crucial to adapt to the environment for some animals, but how the nervous system processes and integrates whisker information is still an open question. It is well-known that two main parallel pathways through Ventral posteromedial thalamic nucleus (VPM) ascend to the barrel cortex, and classical theory suggests that the cross-talk from trigeminal nucleus interpolaris (Sp5i) to principal nucleus (Pr5) between the main parallel pathways contributes to the multi-whisker integration in barrel columns. Moreover, some studies suggest there are other cross-streams between the parallel pathways. To confirm their existence, in this study we used a dual-viral labeling strategy and high-resolution, large-volume light imaging to get the complete morphology of individual VPM neurons and trace their projections. We found some new thalamocortical projections from the ventral lateral part of VPM (VPMvl) to barrel columns. In addition, the retrograde-viral labeling and imaging results showed there were the large trigeminothalamic projections from Sp5i to the dorsomedial section of VPM (VPMdm). Our results reveal new cross-streams between the parallel pathways through VPM, which may involve the execution of multi-whisker integration in barrel columns.

SUBMITTER: Zhang H

PROVIDER: S-EPMC8582278 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Ventral intermediate thalamic deep brain stimulation is a standard therapy for the treatment of medically refractory essential tremor and tremor-dominant Parkinson's disease. Despite the therapeutic benefits, the mechanisms of action are varied and complex, and the pathophysiology and genesis of tremor remain unsubstantiated. This intraoperative study investigated the effects of high frequency microstimulation on both neuronal firing and tremor suppression simultaneously. In each of nine essential tremor and two Parkinson's disease patients who underwent stereotactic neurosurgery, two closely spaced (600 µm) microelectrodes were advanced into the ventral intermediate nucleus. One microelectrode recorded action potential firing while the adjacent electrode delivered stimulation trains at 100 Hz and 200 Hz (2-5 s, 100 µA, 150 µs). A triaxial accelerometer was used to measure postural tremor of the contralateral hand. At 200 Hz, stimulation led to 68 ± 8% (P < 0.001) inhibition of neuronal firing and a 53 ± 5% (P < 0.001) reduction in tremor, while 100 Hz reduced firing by 26 ± 12% (not significant) with a 17 ± 6% (P < 0.05) tremor reduction. The degree of cell inhibition and tremor suppression were significantly correlated (P < 0.001). We also found that the most ventroposterior stimulation sites, closest to the border of the ventral caudal nucleus, had the best effect on tremor. Finally, prior to the inhibition of neuronal firing, microstimulation caused a transient driving of neuronal activity at stimulus onset (61% of sites), which gave rise to a tremor phase reset (73% of these sites). This was likely due to activation of the excitatory glutamatergic cortical and cerebellar afferents to the ventral intermediate nucleus. Temporal characteristics of the driving responses (duration, number of spikes, and onset latency) significantly differed between 100 Hz and 200 Hz stimulation trains. The subsequent inhibition of neuronal activity was likely due to synaptic fatigue. Thalamic neuronal inhibition seems necessary for tremor reduction and may function in effect as a thalamic filter to uncouple thalamo-cortical from cortico-spinal reflex loops. Additionally, our findings shed light on the gating properties of the ventral intermediate nucleus within the cerebello-thalamo-cortical tremor network, provide insight for the optimization of deep brain stimulation technologies, and may inform controlled clinical studies for assessing optimal target locations for the treatment of tremor.

Project description:BackgroundAs the relay centre for processing sensory information, the thalamus may involve in the abnormal sensory procedure caused by cortical spreading depression (CSD). However, few studies have focused on the transient response of thalamus during CSD. Our study aimed to investigate the neuronal activity of mouse thalamus ventral posteromedial nucleus (VPM) during CSD by in vivo micro-endoscopic fluorescence imaging of the genetic calcium probe GCaMP6s expressed in excitatory glutamatergic neurons.MethodsThirty-four transgenic VGluT2-GCaMP6s mice were used in the experiments. An endoscope was inserted into the VPM for image acquisition. CSD was induced by KCl topically applied unilaterally on the cranial dura. Data were acquired in awake (ipsilateral or contralateral VPM, saline instead of KCl, MK-801 treatment) and anaesthetized (isoflurane, pentobarbital) states. Statistical analysis was performed using analysis of variance (ANOVA) by SPSS.ResultsWe found that after CSD induced in ipsilateral motor cortex, the neuronal activity increased and propagated from the posterior-lateral to the anterior-medial part of the VPM with an average speed of 3.47 mm/min. When CSD was induced in visual cortex, the response propagated in opposite direction, from the anterior-medial to the posterior-lateral part of the VPM. Aanaesthetics resulted in the suppression of VPM activation induced by CSD. No significant VPM activation was detected when CSD was induced in contralateral cortex or KCl was replaced by saline. When 5 mM MK-801 was applied to the dura, the electrode failed to record the DC shift of CSD, and there was no significant VPM activation after KCl application.ConclusionCSD induced propagating activation of the ipsilateral VPM in awake mice. The response might correlate to the cortical location where CSD was induced and might be affected by anaesthetics. No significant VPM activation was detected in saline and mk801 experiment results indicated that this VPM activation is due to CSD rather than mouse motion or direct effect of the KCl applying to the intact dura. This finding suggests the potential involvement of thalamus in the migraine auras.

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Cross-Streams Through the Ventral Posteromedial Thalamic Nucleus to Convey Vibrissal Information

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