Skip to main content

Advertisement

SpringerLink
Log in

Properties and axonal trajectories of posterior semicircular canal nerve-activated vestibulospinal neurons

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We studied the axonal projections of vestibulospinal neurons activated from the posterior semicircular canal. The axonal projection level, axonal pathway, and location of the vestibulospinal neurons originating from the PC were investigated in seven decerebrated cats. Selective electrical stimulation was applied to the PC nerve, and extracellular recordings in the vestibular nuclei were performed. The properties of the PC nerve-activated vestibulospinal neurons were then studied. To estimate the neural pathway in the spinal cord, floating electrodes were placed at the ipsilateral (i) and contralateral (c) lateral vestibulospinal tract (LVST) and medial vestibulospinal tract (MVST) at the C1/C2 junction. To elucidate the projection level, floating electrodes were placed at i-LVST and MVST at the C3, T1, and L3 segments in the spinal cord. Collision block test between orthodromic inputs from the PC nerve and antidromic inputs from the spinal cord verified the existence of the vestibulospinal neurons in the vestibular nuclei. Most (44/47) of the PC nerve-activated vestibulospinal neurons responded to orthodromic stimulation to the PC nerve with a short (<1.4 ms) latency, indicating that they were second-order vestibulospinal neurons. The rest (3/47) responded with a longer (≥1.4 ms) latency, indicating the existence of polysynaptic connections. In 36/47 PC nerve-activated vestibulospinal neurons, the axonal pathway was histologically verified to lie in the spinal cord. The axons of 17/36 vestibulospinal neurons projected to the i-LVST, whereas 14 neurons projected to the MVST, and 5 to the c-LVST. The spinal segment levels of projection of these neurons elucidated that the axons of most (15/17) of vestibulospinal neurons passing through the i-LVST reached the L3 segment level; none (0/14) of the neurons passing through the MVST extended to the L3 segment level; most (13/14) of them did not descend lower than the C3 segment level. In relation to the latency and the pathway, 33/36 PC nerve-activated vestibulospinal neurons were second-order neurons, whereas the remaining three were polysynaptic neurons. Of these, 33 second-order vestibulospinal neurons, 16 passed through the i-LVST, while 13 and 4 descended through the MVST and c-LVST, respectively. The remaining three were polysynaptic neurons. Histological analysis showed that most of the PC nerve-activated vestibulospinal neurons were located within a specific area in the medial part of the lateral vestibular nucleus and the rostral part of the descending vestibular nucleus. In conclusion, it was suggested that PC nerve-activated vestibulospinal neurons that were located within a focal area of the vestibular nuclei have strong connections with the lower segments of the spinal cord and are related to postural stability that is maintained by the short latency vestibulospinal reflex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abzug C, Maeda M, Peterson BW, Wilson VJ (1974) Cervical branching of lumbar vestibulospinal axons. J Physiol 243:499–522

    PubMed  CAS  Google Scholar 

  • Akaike T, Fanardjian VV, Ito M, Kumada M, Nakajima H (1973) Electrophysiological analysis of the vestibulospinal reflex pathway of rabbit. I. Classification of tract cells. Exp Brain Res 17:477–496

    PubMed  CAS  Google Scholar 

  • Britton TC, Day BL, Brown P, Rothwell JC, Thompson PD, Marsden CD (1993) Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man. Exp Brain Res 94:143–151

    Article  PubMed  CAS  Google Scholar 

  • Fukushima K, Peterson BW, Wilson VJ (1979) Vestibulospinal, reticulospinal and interstitiospinal pathways in the cat. Prog Brain Res 50:121–136

    Article  PubMed  CAS  Google Scholar 

  • Hagiwara A, Uchino Y, Sato H, Meng H, Suzuki M (2000) Axonal pathway and projection levels of vestibulospinal neurons activated by posterior semicircular canal. Equilib Res 59:579–585

    Google Scholar 

  • Ikegami H, Sasaki M, Uchino Y (1994) Connections between utricular nerve and neck flexor motoneurons of decerebrate cats. Exp Brain Res 98:373–378

    Article  PubMed  CAS  Google Scholar 

  • Isu N, Uchino Y, Nakashima H, Satoh S, Ichikawa T, Watanabe S (1988) Axonal trajectories of posterior canal-activated secondary vestibular neurons and their coactivation of extraocular and neck flexor motoneurons in the cat. Exp Brain Res 70:181–191

    PubMed  CAS  Google Scholar 

  • Kitajima N, Sugita-Kitajima A, Bai R, Sasaki M, Sato H, Imagawa M, Kawamoto E, Suzuki M, Uchino Y (2006) Axonal pathways and projection levels of anterior semicircular canal nerve-activated vestibulospinal neurons in cats. Neurosci Lett 406:1–5

    Article  PubMed  CAS  Google Scholar 

  • Kushiro K, Zakir M, Ogawa Y, Sato H, Uchino Y (1999) Saccular and utricular inputs to sternocleidomastoid motoneurons of decerebrate cats. Exp Brain Res 126:410–416

    Article  PubMed  CAS  Google Scholar 

  • Kuze B, Matsuyama K, Matsui T, Miyata H, Mori S (1999) Segment-specific branching patterns of single vestibulospinal tract axons arising from the lateral vestibular nucleus in the cat: a PHA-L tracing study. J Comp Neurol 414:80–96

    Article  PubMed  CAS  Google Scholar 

  • Mannen H, Sasaki S, Ishizuka N (1982) Trajectory of primary vestibular fibers originating from the lateral, anterior, and posterior semicircular canals in the cat. Proc Jpn Acad Ser B 58:237–242

    Article  Google Scholar 

  • Mitsacos A, Reisine H, Highstein SM (1983) The superior vestibular nucleus: an intracellular HRP study in the cat. I. Vestibulo-ocular neurons. J Comp Neurol 215:78–91

    Article  PubMed  CAS  Google Scholar 

  • Muto N, Shinomiya K, Komori H, Mochida K, Furuya K (1995) Spinal cord monitoring of the ventral funiculus function. Analysis of spinal field potentials after galvanic vestibular stimulation. Spine 20:2429–2434 discussion 2435

    Article  PubMed  CAS  Google Scholar 

  • Precht W, Shimazu H (1965) Functional connections of tonic and kinetic vestibular neurons with primary vestibular afferents. J Neurophysiol 28:1014–1028

    PubMed  CAS  Google Scholar 

  • Rapoport S, Susswein A, Uchino Y, Wilson VJ (1977) Properties of vestibular neurones projecting to neck segments of the cat spinal cord. J Physiol 268:493–510

    PubMed  CAS  Google Scholar 

  • Sasaki M, Hiranuma K, Isu N, Uchino Y (1991) Is there a three neuron arc in the cat utriculo-trochlear pathway? Exp Brain Res 86:421–425

    Article  PubMed  CAS  Google Scholar 

  • Sato H, Endo K, Ikegami H, Imagawa M, Sasaki M, Uchino Y (1996) Properties of utricular nerve-activated vestibulospinal neurons in cats. Exp Brain Res 112:197–202

    Article  PubMed  CAS  Google Scholar 

  • Sato H, Imagawa M, Isu N, Uchino Y (1997) Properties of saccular nerve-activated vestibulospinal neurons in cats. Exp Brain Res 116:381–388

    Article  PubMed  CAS  Google Scholar 

  • Sato H, Imagawa M, Kushiro K, Zakir M, Uchino Y (2000) Convergence of posterior semicircular canal and saccular inputs in single vestibular nuclei neurons in cats. Exp Brain Res 131:253–261

    Article  PubMed  CAS  Google Scholar 

  • Shinoda Y, Ohgaki T, Sugiuchi Y, Futami T, Kakei S (1992) Functional synergies of neck muscles innervated by single medial vestibulospinal axons. Ann NY Acad Sci 656:507–518

    Article  PubMed  CAS  Google Scholar 

  • Shinoda Y, Sugiuchi Y, Futami T, Ando N, Kawasaki T (1994) Input patterns and pathways from the six semicircular canals to motoneurons of neck muscles. I. The multifidus muscle group. J Neurophysiol 72:2691–2702

    PubMed  CAS  Google Scholar 

  • Sugita A, Bai R, Imagawa M, Sato H, Sasaki M, Kitajima N, Koizuka I, Uchino Y (2004) Properties of horizontal semicircular canal nerve-activated vestibulospinal neurons in cats. Exp Brain Res 156:478–486

    Article  PubMed  Google Scholar 

  • Suzuki JI, Cohen B (1964) Head, eye, body and limb movements from semicircular canal nerves. Exp Neurol 10:393–405

    Article  PubMed  CAS  Google Scholar 

  • Thomas RC, Wilson VJ (1965) Precise localization of Renshaw cells with a new marking technique. Nature 206:211–213

    Article  PubMed  CAS  Google Scholar 

  • Uchino Y, Sato H, Sasaki M, Imagawa M, Ikegami H, Isu N, Graf W (1997) Sacculocollic reflex arcs in cats. J Neurophysiol 77:3003–3012

    PubMed  CAS  Google Scholar 

  • Watson SR, Colebatch JG (1998) Vestibular-evoked electromyographic responses in soleus: a comparison between click and galvanic stimulation. Exp Brain Res 119:504–510

    Article  PubMed  CAS  Google Scholar 

  • Wilson VJ, Melvill-Jones G (1976) Mammalian vestibular physiology. Plenum Press, New York

    Google Scholar 

  • Zakir M, Kushiro K, Ogawa Y, Sato H, Uchino Y (2000) Convergence patterns of the posterior semicircular canal and utricular inputs in single vestibular neurons in cats. Exp Brain Res 132:139–148

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. M. Sasaki, Dr. H. Sato, and Ms. M. Imagawa for technical contribution and Ms. K. Takayama for secretarial assistance. This study was supported by a research grant from the Japan Space Forum promoted by NASDA (National Space Development Agency of Japan). K.K. was supported in part by the Global COE Program “Revitalizing Education for Dynamic Hearts and Minds,” MEXT, Japan.

Author information

Authors and Affiliations

  1. Department of Human and Environmental Studies, Kyoto University, Yoshida-nihonmatsu-cho, Sakyo-ku, Kyoto, 606-8501, Japan

    Keisuke Kushiro

  2. Department of Physiology, Tokyo Medical University, 6-1-1 Shinjuku, Shinjuku-ku, Tokyo, 160-8402, Japan

    Rishu Bai, Naoharu Kitajima, Akemi Sugita-Kitajima & Yoshio Uchino

  3. Department of Otolaryngology, Tokyo Medical University, 6-7-1 Nishishinjuku, Shinjuku-ku, Tokyo, 160-0023, Japan

    Naoharu Kitajima

  4. Department of Otolaryngology, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae-ku, Kawasaki, Kanagawa, 216-8511, Japan

    Akemi Sugita-Kitajima

  5. Health Service Facility for the Elderly, “Green Village Angyo,” 1145 Angyo, Kawaguchi, Saitama, 334-0059, Japan

    Yoshio Uchino

Authors
  1. Keisuke Kushiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rishu Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naoharu Kitajima
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akemi Sugita-Kitajima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshio Uchino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Keisuke Kushiro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kushiro, K., Bai, R., Kitajima, N. et al. Properties and axonal trajectories of posterior semicircular canal nerve-activated vestibulospinal neurons. Exp Brain Res 191, 257–264 (2008). https://doi.org/10.1007/s00221-008-1503-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-008-1503-9

Keywords

Search

Navigation