Skip to main content
Log in

Vestibular influences on CA1 neurons in the rat hippocampus: an electrophysiological study in vivo

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

Abstract

Vestibular information is known to be important for accurate spatial orientation and navigation. Hippocampal place cells, which appear to encode an animal’s location within the environment, are also thought to play an essential role in spatial orientation. Therefore, it can be hypothesized that vestibular information may influence cornu ammonis region 1 (CA1) hippocampal neuronal activity. To explore this possibility, the effects of electrical stimulation of the medial vestibular nucleus (MVN) on the firing rates of hippocampal CA1 neurons in the urethane-anesthetized rat were investigated using extracellular single unit recordings. The firing rates of CA1 complex spike cells (n=29), which most likely correspond to place cells, consistently increased during electrical stimulation of the MVN in a current intensity dependent manner. Stimulation applied adjacent to the MVN failed to elicit a response. Overall, the firing rates of non-complex spike cells (n=22) did not show a consistent response to vestibular stimulation, although in some cells clear responses to the stimulation were observed. These findings suggest that vestibular inputs may contribute to spatial information processing in the hippocampus.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a–d
Fig. 2a, b
Fig. 3

Similar content being viewed by others

References

  • Berthoz A, Isräel I, Georges-Francois P, Grasso R, Tsuzuku T (1995) Spatial memory of body linear displacement: what is being stored? Science 269:95–98

    CAS  PubMed  Google Scholar 

  • Cuthbert PC, Gilchrist DP, Hicks SL, MacDougall HG, Curthoys IS (2000) Electrophysiological evidence for vestibular activation of the guinea pig hippocampus. Neuroreport 11:1443–1447

    CAS  PubMed  Google Scholar 

  • Fox SE, Ranck JB Jr (1981) Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp Brain Res 41:399–410

    CAS  PubMed  Google Scholar 

  • Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470

    Article  CAS  PubMed  Google Scholar 

  • Horii A, Takeda N, Mochizuki T, Okakura-Mochizuki K, Yamamoto Y, Yamatodani A (1994) Effects of vestibular stimulation on acetylcholine release from rat hippocampus: an in vivo microdialysis study. J Neurophysiol 72:605–611

    CAS  PubMed  Google Scholar 

  • Liu P, King J, Zheng Y, Darlington CL, Smith PF (2003a) Nitric oxide synthase and arginase expression in the vestibular nucleus and hippocampus following unilateral vestibular deafferentation in the rat. Brain Res 966:19–25

    Article  CAS  PubMed  Google Scholar 

  • Liu P, King J, Zheng Y, Darlington CL, Smith PF (2003b) Long-term changes in hippocampal NMDA receptors following peripheral vestibular damage. Neuroscience 117:965–970

    Article  CAS  PubMed  Google Scholar 

  • Mathews BL, Ryu JH, Bockaneck C (1989) Vestibular contribution to spatial orientation: evidence of vestibular navigation in an animal model. Acta Otolaryngol (Stockh) Suppl 468:149–154

    Google Scholar 

  • O’Keefe J (1979) A review of the hippocampal place cells. Prog Neurobiol 13:419–439

    CAS  PubMed  Google Scholar 

  • O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175

    CAS  PubMed  Google Scholar 

  • O’Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–330

    CAS  PubMed  Google Scholar 

  • O’Mara SM, Rolls ET, Berthoz A, Kesner RP (1994) Neurons responding to whole-body motion in the primate hippocampus. J Neurosci 14:6511–6523

    CAS  PubMed  Google Scholar 

  • Ossenkopp KP, Hargreaves EL (1993) Spatial learning in an enclosed eight-arm radial maze in rats with sodium arsanilate-induced labyrinthectomies. Behav Neural Biol 59:253–257

    CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic Press, Orlando

  • Péruch P, Borel L, Gaunet F, Thinus-Blanc G, Magnan J, Lacour M (1999) Spatial performance of unilateral vestibular defective patients in nonvisual versus visual navigation. J Vestibular Res 9:37–47

    Google Scholar 

  • Petrosini L (1984) Task-dependent rate of recovery from hemilabyrinthectomy: an analysis of swimming and locomotor performances. Physiol Behav 33:799–804

    Article  CAS  PubMed  Google Scholar 

  • Russell NA (2002) Vestibular contributions to hippocampal function. PhD thesis, University of Otago, Dunedin, New Zealand

  • Russell NA, Liu P, Darlington CL, Bilkey DK, Horii A, Smith PF (2001) Hippocampal theta rhythm has decreased power in rats with bilateral vestibular labyrinthectomies. Int J Neurosci 109:212

    Google Scholar 

  • Russell NA, Horii A, Smith PF, Darlington CL, Bilkey DK (2003) Long-term effects of permanent vestibular lesions on hippocampal spatial firing. J Neurosci 23:6490–6498

    CAS  PubMed  Google Scholar 

  • Russell NA, Horii A, Smith PF, Darlington CL, Bilkey DK (in press) Bilateral peripheral vestibular lesions produce long-term changes in spatial learning in the rat. J Vestibular Res

  • Semba K, Reiner PB, McGeer EG, Fibiger HC (1988) Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 267:433–453

    CAS  PubMed  Google Scholar 

  • Sharp PE, Blair HT, Etkin D, Tzanetos DB (1995) Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells. J Neurosci 15:173–189

    CAS  PubMed  Google Scholar 

  • Smith PF (1997) Vestibular-hippocampal interactions. Hippocampus 7:465–471

    CAS  PubMed  Google Scholar 

  • Stackman RW, Herbert AM (2002) Rats with lesions of the vestibular system require a visual landmark for spatial navigation. Behav Brain Res 128:27–40

    Article  PubMed  Google Scholar 

  • Stackman RW, Clark AS, Taube JS (2002) Hippocampal spatial representations require vestibular input. Hippocampus 12:291–303

    Article  PubMed  Google Scholar 

  • Taube JS, Goodridge JP, Golob EJ, Dudchenko PA, Stackman RW (1996) Processing the head direction cell signal: a review and commentary. Brain Res Bull 40:477–486

    CAS  PubMed  Google Scholar 

  • Tehovnik EJ (1996) Electrical stimulation of neural tissue to evoke behavioral responses. J Neurosci Methods 65:1–17

    Article  CAS  PubMed  Google Scholar 

  • Vertes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal controlling the theta rhythm of the hippocampus. Neuroscience 81:893–926

    CAS  PubMed  Google Scholar 

  • Zheng Y, Smith PF, Darlington CL (1999a) Subregional analysis of amino acid levels in the guinea pig hippocampus following unilateral vestibular deafferentation. J Vestibular Res 9:335–345

    CAS  Google Scholar 

  • Zheng Y, Smith PF, Darlington CL (1999b) Noradrenaline and serotonin levels in the guinea pig hippocampus following unilateral vestibular deafferentation. Brain Res 836:199–202

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Horii A, Appleton I, Darlington CL, Smith PF (2001) Damage to the vestibular inner ear causes long-term changes in neuronal nitric oxide synthase expression in the rat hippocampus. Neuroscience 105:1–5

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from the Marsden Fund (to DKB), the New Zealand Neurological Foundation (to PFS and CLD), and the Health Research Council of New Zealand (to PFS and CLD). AH continued to receive support from Osaka University Medical School while on leave from that institution.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arata Horii.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Horii, A., Russell, N.A., Smith, P.F. et al. Vestibular influences on CA1 neurons in the rat hippocampus: an electrophysiological study in vivo. Exp Brain Res 155, 245–250 (2004). https://doi.org/10.1007/s00221-003-1725-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-003-1725-9

Keywords

Navigation