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Activation of the thalamic parafascicular nucleus by electrical stimulation of the peripheral vestibular nerve in rats

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Abstract

The parafascicular nucleus (PFN) of the thalamus is a primary structure in the feedback circuit of the basal ganglia-thalamo-cortical system, as well as in the neural circuit of the vestibulo-thalamo-striatal pathway. We investigated the characteristics of the functional connectivity between the peripheral vestibular system and the PFN in rats. A single electrical stimulation was applied to the horizontal semicircular canal nerve in the peripheral vestibular end-organs. This resulted in polysynaptic local field potentials (LFPs) in the PFN, which were composed of long-lasting multiple waves. The LFPs were prominently seen contralateral to the stimulation site. The PFN LFPs were suppressed by transient chemical de-afferentation of peripheral vestibular activity using a 5% lidocaine injection into the middle ear. The spontaneous firing rate of the single units increased after electrical stimulation to the horizontal canal nerve in a frequency-dependent manner. The induction of cFos protein was more prominent in the contralateral PFN than in the ipsilateral PFN following horizontal semicircular canal nerve stimulation. The functional vestibulo-parafascicular connection is a neural substrate for the transmission of vestibular sensory information to the basal ganglia.

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Acknowledgements

This work was supported by a grant from the Korea Basic Science Institute (D35401).

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Authors and Affiliations

  1. Department of Physiology, Wonkwang University School of Medicine and Brain Science Institute at Wonkwang University, Iksan, 570-749, Korea

    Nari Kim, Myoung Ae Choi, Ho Koo, Byung Rim Park, Sang Who Han & Min Sun Kim

  2. Division of Radiation Oncology, Korea Institute of Radiological and Medical Sciences, Seoul, 139-706, Korea

    Nari Kim

  3. Division of Convergence Biotechnology, Korea Basic Science Institute, Cheongju, Chungbook, 28119, Korea

    Chaejoon Cheong

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  1. Nari Kim
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  2. Myoung Ae Choi
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  3. Ho Koo
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  4. Byung Rim Park
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  6. Chaejoon Cheong
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Correspondence to Min Sun Kim.

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Ethical approval

All experimental procedures were conducted under a protocol approved by the Institutional Animal Care and Use Committee of Wonkwang University and in accordance with WKU12-61.

Electronic supplementary material

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221_2016_4864_MOESM1_ESM.pdf

Supplementary Fig. 1. Typical changes in single-unit activity in the PFN in response to 30 repetitive stimuli of 5 train pulses for 30 s (a) and continuous 200-Hz stimulation for 30 s (b). Spontaneous firing of PFN neurons was minimally changed by 30 repetitive stimulations of 5 train pulses with a 20-ms interval. In contrast, 200 Hz continuous stimulation caused an increase in the spontaneous firing of PFN neurons (PDF 31 KB)

221_2016_4864_MOESM2_ESM.pdf

Supplementary Fig. 2. Expressions of cFos-IL neurons at different rostrocaudal levels of the PFN of sham-treated animal, which did not receive the stimulation, and in the PFN 90 min following HSC nerve stimulation. The photographs were captured at -4.1-, -4.2-, and − 4.3-mm AP, respectively. The expression of cFos-IL neurons mainly occurred in PFN subregions between AP -4.1 mm and AP -4.2 mm. Ipsi, ipsilateral; Contra, contralateral; fr, fasciculus retroflexus; and Po, posterior thalamic nuclear group. Scale bar = 500 µm (PDF 825 KB)

221_2016_4864_MOESM3_ESM.pdf

Supplementary Fig. 3. Regional distribution of cFos-IL neurons in the contralateral other thalamic nuclei of sham-treated animal and of animal with HSC stimulation. There was a significant increase in cFos-IL neuron expression in the posterior thalamic nuclear group (Po), the ventral posteromedial thalamic nucleus (VPM), and the medial habenular nucleus (MHb) 90 min following HSC nerve stimulation. LPLR, lateral posterior thalamic nucleus, laterorostral; VPL, ventral posterolateral thalamic nucleus; VG1, ventral geniculate nucleus layer 1; fr, fasciculus retroflexus. Scale bar = 500 µm (PDF 154 KB)

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Kim, N., Choi, M.A., Koo, H. et al. Activation of the thalamic parafascicular nucleus by electrical stimulation of the peripheral vestibular nerve in rats. Exp Brain Res 235, 1617–1625 (2017). https://doi.org/10.1007/s00221-016-4864-5

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