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Acta Biologica Hungarica

, Volume 59, Issue 3, pp 269–279 | Cite as

Modality Distribution of Sensory Neurons in the Feline Caudate Nucleus and the Substantia Nigra

  • Zita Márkus
  • Gábriella Eördegh
  • Zsuzsanna Paróczy
  • G. Benedek
  • A. NagyEmail author
Article

Abstract

Despite extensive analysis of the motor functions of the basal ganglia and the fact that multisensory information processing appears critical for the execution of their behavioral action, little is known concerning the sensory functions of the caudate nucleus (CN) and the substantia nigra (SN). In the present study, we set out to describe the sensory modality distribution and to determine the proportions of multisensory units within the CN and the SN. The separate single sensory modality tests demonstrated that a majority of the neurons responded to only one modality, so that they seemed to be unimodal. In contrast with these findings, a large proportion of these neurons exhibited significant multisensory cross-modal interactions. Thus, these neurons should also be classified as multisensory. Our results suggest that a surprisingly high proportion of sensory neurons in the basal ganglia are multisensory, and demonstrate that an analysis without a consideration of multisensory cross-modal interactions may strongly underrepresent the number of multisensory units. We conclude that a majority of the sensory neurons in the CN and SN process multisensory information and only a minority of these units are clearly unimodal.

Keywords

Visual auditory somatosensory multisensory integration basal ganglia 

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References

  1. 1.
    Barneoud, J., Descombris, E., Aubin, N., Abrous, D. N. (2000) Evaluation of simple and complex sensorimotor behaviours in rats with a partial lesion of the dopaminergic nigrostriatal system. Eur. J. Neurosci. 12, 322–336.CrossRefGoogle Scholar
  2. 2.
    Benedek, G., Eördegh, G., Chadaide, Z., Nagy, A. (2004) Distributed population coding of multi-sensory spatial information in the associative cortex. Eur. J. Neurosci. 29, 525–529.CrossRefGoogle Scholar
  3. 3.
    Brown, L. L., Schneider, J. S., Lidsky, T. I. (1997) Sensory and cognitive functions of the basal ganglia. Curr Opin. Neurobiol. 7, 157–163.CrossRefGoogle Scholar
  4. 4.
    Chudler, E. H., Sugiyama, K., Dong, W. K. (1995) Multisensory convergence and integration in the neostriatum and globus pallidus of the rat. Brain Res. 674, 33–45.CrossRefGoogle Scholar
  5. 5.
    Harting, J. K., Updyke, B. V., Van Lieshout, D. P. (2001) Striatal projections from the cat visual thalamus. Eur. J. Neurosci. 14, 893–896.CrossRefGoogle Scholar
  6. 6.
    Harting, J. K., Updyke, B. V., Van Lieshout, D. P. (2001) The visual-oculomotor striatum of the cat: functional relationship to the superior colliculus. Exp. Brain Res. 136, 138–142.CrossRefGoogle Scholar
  7. 7.
    Hikosaka, O., Sakamoto, M., Usui, S. (1989) Functional properties of monkey caudate neurons. II. Visual and auditory responses. J. Neurophysiol. 61, 799–813.CrossRefGoogle Scholar
  8. 8.
    Hikosaka, O., Wurtz, R. H. (1983) Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J. Neurophysiol. 49, 1230–1253.CrossRefGoogle Scholar
  9. 9.
    Joseph, J. P., Boussaoud, D. (1985) Role of the cat substantia nigra pars reticulata in eye and head movements. I. Neural activity. Exp. Brain Res. 57, 286–296.CrossRefGoogle Scholar
  10. 10.
    King, A. J., Palmer, A. R. (1985) Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus. Exp. Brain Res. 60, 492–500.CrossRefGoogle Scholar
  11. 11.
    Lynd-Balta, E., Haber, S. N. (1994) The organization of midbrain projections to the striatum in the primate: sensorimotor-related striatum versus ventral striatum. Neuroscience 59, 625–640.CrossRefGoogle Scholar
  12. 12.
    Magarinos-Ascone, C., Garcia-Austt, E., Buno, W. (1994) Polymodal sensory and motor convergence in substantia nigra neurons of the awake monke. Brain Res. 646, 299–302.CrossRefGoogle Scholar
  13. 13.
    Meredith, M. A., Stein, B. E. (1983) Interactions among converging sensory inputs in the superior colliculus. Science 221, 389–391.CrossRefGoogle Scholar
  14. 14.
    Meredith, M. A., Stein, B. E. (1986) Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. J. Neurophysiol. 56, 640–662.CrossRefGoogle Scholar
  15. 15.
    Nagy, A., Eördegh, G., Norita, M., Benedek, G. (2003) Visual receptive field properties of neurons in the caudate nucleus. Eur. J. Neurosci. 18, 449–452.CrossRefGoogle Scholar
  16. 16.
    Nagy, A., Eördegh, G., Norita, M., Benedek, G. (2005) Visual receptive field properties of excitatory neurons in the substantia nigra. Neuroscience 150, 513–518.CrossRefGoogle Scholar
  17. 17.
    Nagy, A., Paröczy, Z., Norita, M., Benedek, G. (2005) Multisensory responses and receptive field properties of neurons in the substantia nigra and in the caudate nucleus. Eur. J. Neurosci. 22, 419–424.CrossRefGoogle Scholar
  18. 18.
    Nagy, A., Eördegh, G., Paröczy, Z., Markus, Z., Benedek, G. (2006) Multisensory integration in the basal ganglia. Eur. J. Neurosci. 24, 917–924.CrossRefGoogle Scholar
  19. 19.
    Pouderoux, C., Freton, E. (1979) Patterns of unit responses to visual stimuli in the cat caudate nucleus under chloralose anesthesia. Neurosci. Lett. 11, 53–58.CrossRefGoogle Scholar
  20. 20.
    Schneider, J. S. (1991) Responses of striatal neurons to peripheral sensory stimulation in symptomatic MPTP-exposed cats. Brain Res. 544, 297–302.CrossRefGoogle Scholar
  21. 21.
    Schwarz, M., Sontag, K. H., Wand, P. (1984) Sensory-motor processing in substantia nigra pars reticulata in conscious cats. J. Physiol. 347, 129–147.CrossRefGoogle Scholar
  22. 22.
    Snider, R. S., Niemer, W. T (1964) The Stereotaxic Atlas of the Cat Brain. University of Chicago Press, Chicago.Google Scholar
  23. 23.
    Stein, B. E. (1998) Neural mechanisms for synthesizing sensory information and producing adaptive behaviours. Exp. Brain Res. 123, 124–135.CrossRefGoogle Scholar
  24. 24.
    Strecker, E. R., Steinfels, G., Abercrombie, E. D., Jacobs, B. L. (1985) Caudate unit activity in freely moving cats: effects of phasic auditory and visual stimuli. Brain Res. 329, 350–353.CrossRefGoogle Scholar
  25. 25.
    Villeneuve, M. Y., Casanova, C. (2003) On the use of isoflurane versus halothane in the study of visual response properties of single cells in the primary visual cortex. J. Neurosci. Meth. 129, 19–31.CrossRefGoogle Scholar
  26. 26.
    Wallace, M. T., Meredith, M. A., Stein, B. E. (1998) Multisensory integration in the superior colliculus of the alert cat. J. Neurophysiol. 80, 1006–1010.CrossRefGoogle Scholar
  27. 27.
    Wallace, M. T., Meredith, M. A., Stein, B. E. (1992) Integration of multiple sensory modalities in cat cortex. Exp. Brain Res. 91, 484–488.CrossRefGoogle Scholar
  28. 28.
    Wallace, M. T., Stein, B. E. (1996) Sensory organization of the superior colliculus in cat and monkey. Prog. Brain Res. 112, 301–311.CrossRefGoogle Scholar
  29. 29.
    Wallace, M. T., Wilkinson, L. K., Stein, B. E. (1996) Representation and integration of multiple sensory inputs in primate superior colliculus. J. Neurophysiol. 76, 1246–1266.CrossRefGoogle Scholar
  30. 30.
    Wilson, J. S., Hull, C. D., Buchwald, N. A. (1983) Intracellular studies of the convergence of sensory input on caudate neurons of cat. Brain Res. 270, 197–208.CrossRefGoogle Scholar

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© Akadémiai Kiadó, Budapest 2008

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Zita Márkus
    • 1
  • Gábriella Eördegh
    • 1
  • Zsuzsanna Paróczy
    • 1
  • G. Benedek
    • 1
  • A. Nagy
    • 1
    Email author
  1. 1.Department of Physiology, Faculty of Medicine, Albert Szent-Györgyi Medical and Pharmaceutical CentreUniversity of SzegedSzegedHungary

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