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

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.

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.

    CAS  Article  Google 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.

    Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google Scholar 

  13. 13.

    Meredith, M. A., Stein, B. E. (1983) Interactions among converging sensory inputs in the superior colliculus. Science 221, 389–391.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to A. Nagy.

Rights and permissions

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.

Reprints and Permissions

About this article

Cite this article

Márkus, Z., Eördegh, G., Paróczy, Z. et al. Modality Distribution of Sensory Neurons in the Feline Caudate Nucleus and the Substantia Nigra. BIOLOGIA FUTURA 59, 269–279 (2008). https://doi.org/10.1556/ABiol.59.2008.3.1

Download citation

Keywords

  • Visual
  • auditory
  • somatosensory
  • multisensory integration
  • basal ganglia