Responses of Tonic Striatal Neurons to Conditioned Stimuli in Behaving Monkeys

Coding of an Associated Behavioral Reaction or Expectation of Reward?
  • Paul Apicella
  • Eric Legallet
  • Elisabeth Trouche
Part of the Advances in Behavioral Biology book series (ABBI, volume 47)

Summary

Previous studies have shown that tonically discharging neurons in monkey striatum can be modulated by the onset of external stimuli, which are reliable predictors of a rewarding event. In this study, we investigated the responses of tonic neurons to visual stimuli presented in advance of the delivery of reward or without any subsequent reward. A total number of 158 tonic neurons with typical electrophysiological characteristics was recorded in the caudate nucleus and putamen of two monkeys under two behavioral conditions: (1) an active one, in which a specific arm movement triggered by a visual stimulus had to be performed to obtain a reward, (2) a passive one, in which a visual stimulus was consistently and automatically followed by a reward. With each of these conditions, the non-rewarded trials were run in separate sessions to check whether there were any reward-specific effects. Most of the neurons responded to the stimuli associated with reward both during the active and the passive conditions, suggesting that the responses were not specific to the type of behavioral reaction to be initiated. In some responding neurons, the responses remained present in the nonperforming condition when a stimulus not followed by the reward was repeatedly presented. Responses could also occur in the task performance condition when the stimulus was presented at a point that was out of the monkey’s reach. The fact that neuronal responses persisted in conditions in which the animal knew that he would not get a reward after detecting a stimulus suggests that the responses observed here were not specifically dependent on the reward components of the behavioral conditions. These results indicate that although there exist several lines of evidence showing that tonic striatal neurons respond to stimuli eliciting immediate behavioral reactions and predicting that a reward is forthcoming, these neurons may be involved in some more general aspects of the animals’ reactivity to environmental stimuli in a behavioral context.

Keywords

Conditioned Stimulus Visual Stimulus Caudate Nucleus Neuronal Response Passive Condition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alexander, G. E., and DeLong, M. R., 1985, Microstimulation of the primate neostriatum. I. Physiological properties of striatal microexcitable zones, J. Neurophysiol. 53: 1401–1416.PubMedGoogle Scholar
  2. Aosaki, T., Graybiel, A. M., and Kimura, M., 1995a, Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys, Science 265: 412–415.CrossRefGoogle Scholar
  3. Aosaki, T., Kimura, M, and Graybiel, A. M., 1995b, Temporal and spatial characteristics of tonically active neurons of the primate’s striatum, J. Neurophysiol. 73: 1234–1252.PubMedGoogle Scholar
  4. Aosaki, T., Tsubokawa, H., Ishida, A., Watanabe, K., Graybiel, A. M., and Kimura, M., 1994, Responses of tonically active neurons in the primate’s striatum undergo systematic changes during behavioral sensorimotor conditioning, J. Neurosci. 14: 3969–3984.PubMedGoogle Scholar
  5. Apicella, P., Schultz, W., and Scarnati, E., 1991, Tonically discharging neurons of monkey striatum respond to preparatory and rewarding stimuli, Exp. Brain Res. 84: 672–675.PubMedCrossRefGoogle Scholar
  6. Apicella, P., Legallet, E., and Trouche, E., 1995, Responses of tonically discharging neurons in monkey striatum to visual stimuli presented under passive conditions and during task performance, Neurosci. Lett. (submitted).Google Scholar
  7. Graybiel, A. M, Aosaki, T., Flaherty, A. W., and Kimura, M., 1994, The basal ganglia and adaptive motor control, Science 265: 1826–1831.PubMedCrossRefGoogle Scholar
  8. Hikosaka, O., Sakamoto, M., and Usui, S., 1989, Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements, J. Neurophysiol. 61: 780–798.PubMedGoogle Scholar
  9. Kawaguchi, Y., 1992, Large aspiny cells in the matrix of the rat neostriatum in vitro: Physiological identification, relation to the compartments and excitatory postsynaptic currents, J. Neurophysiol. 67: 1669–1682.PubMedGoogle Scholar
  10. Kimura, M., Rajkowski, J., and Evarts, E. V., 1984, Tonically discharging putamen neurons exhibit set dependent responses, Proc. Natl. Acad. Sci. USA 81: 4998–5001.PubMedCrossRefGoogle Scholar
  11. Kimura, M., 1986, The role of primate putamen neurons in the association of sensory stimuli with movement, Neurosci. Res. 3: 436–443.PubMedCrossRefGoogle Scholar
  12. Kimura, M., 1992, Behavioral modulation of sensory responses of primate putamen neurons, Brain Res. 578: 204–214.PubMedCrossRefGoogle Scholar
  13. Wilson, C. J., Chang, H. T., and Kitai, S. T., 1990, Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum, J. Neurosci. 10: 508–519.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Paul Apicella
    • 1
  • Eric Legallet
    • 1
  • Elisabeth Trouche
    • 1
  1. 1.Laboratoire de Neurobiologie Cellulaire et FonctionnelleCNRSMarseille cedex 20France

Personalised recommendations