Tonically Active Neurons in the Monkey Striatum are Sensitive to Sensory Events in a Manner that Reflects their Predictability in Time

  • Paul Apicella
  • Sabrina Ravel
  • Pierangelo Sardo
  • Eric Legallet
Part of the Advances in Behavioral Biology book series (ABBI, volume 54)


It is now well established that tonically active neurons (TANs) in the monkey striatum respond to motivationally relevant sensory events, such as conditioned stimuli to which the animal had to react correctly to obtain reward. Recent findings obtained in our laboratory suggested that stimulus prediction may influence the responsiveness of the TANs. In the present study we specifically investigated the effects of temporal aspects of prediction on the responses of single TANs recorded both in the caudate nucleus and putamen of two macaque monkeys. Three different behavioral situations were employed: (1) an instrumental task, in which a visual stimulus triggering a rewarded movement was preceded by an instruction stimulus presented at a fixed interval of 1.5 s before the trigger onset; (2) a classically conditioned task, in which a visual stimulus was followed after a fixed interval of 1 s by the delivery of a liquid reward without requiring the monkey to react to the stimulus; (3) a free reward condition, in which a liquid reward was delivered at unpredictable times (5.5–8.5 s). Both monkeys received extensive training on the two tasks having a fixed time interval between the predictive cue and the trigger stimulus or reward. To study the effect of changes in the temporal predictability of stimuli, the interval between instruction and trigger stimuli was prolonged to 4.5 s in the instrumental task and the reward was given earlier (0.3 s) or later (2 s) than its usual time of delivery in the classically conditioned task. The percentage of TANs showing responses was increased when stimuli were less predictable in time, compared to the situations in which the onset time of stimuli was highly predictable. Responses to reward given outside of any task were reduced with repeated liquid delivery at the same 2 s intervals, further suggesting that the temporal predictability of stimuli was an important factor for eliciting neuronal responses. The present results demonstrate that the efficacy of stimuli to modulate the string of TANs is determined both by the motivational relevance of stimuli and by predictions about stimulus timing.


Conditioned Stimulus Sensory Event Experimental Brain Research Conditioned Task Temporal Predictability 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alexander, G. E. & DeLong, M. R. (1985) Microstimulation of the primate neostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties.Journal of Neurophysiology 531417–1430.PubMedGoogle Scholar
  2. Aosaki, T., Tsubokawa, H., Ishida, A., Watanabe, K., Graybiel, A. M. & Kimura, M. (1994) Responses of tonically active neurons in the primate’s striatum undergo systematic changes during behavioral sensorimotor conditioning.Journal of Neuroscience14, 3969–3984.PubMedGoogle Scholar
  3. Aosaki, T., Kimura, M. & Graybiel, A. M. (1995) Temporal and spatial characteristics of tonically active neurons of the primate’s striatum.Journal of Neurophysiology73, 1234–1252.PubMedGoogle Scholar
  4. Apicella, P., Schultz, W. & Scamati, E. (1991) Tonically discharging neurons of monkey striatum respond to preparatory and rewarding stimuli.Experimental Brain Research84, 672–675.CrossRefGoogle Scholar
  5. Apicella, P., Legallet, E. & Trouche, E. (1996) Responses of tonically discharging neurons in monkey striatum to visual stimuli presented under passive conditions and during task performance.Neuroscience Letters203, 147–150.PubMedCrossRefGoogle Scholar
  6. Apicella, P., Legallet, E. & Trouche, E. (1997) Responses of tonically discharging neurons in the monkey striatum to primary rewards delivered during different behavioral states.Experimental Brain Research116, 456–466.CrossRefGoogle Scholar
  7. Apicella, P., Ravel, S., Sardo, P. & Legallet, E. (1998) Influence of predictive information on responses of tonically active neurons in the monkey striatum.Journal of Neurophysiology80, 3341–3344.PubMedGoogle Scholar
  8. Graybiel, A. M. (1995) Building action repertoires: memory and learning functions of the basal ganglia.Current Opinion in Neurobiology5,733–741.PubMedCrossRefGoogle Scholar
  9. Graybiel, A. M., Aosaki, T., Flaherty, A. W. & Kimura, M. (1994) The basal ganglia and adaptive motor control.Science265, 1826–1831.PubMedCrossRefGoogle Scholar
  10. Harrington, D. L., York Haaland, K., Yeo, R. A. & Marder, E. (1990) Procedural memory in Parkinson’s disease. Impaired motor but not visuoperceptual learning.Journal of Clinical and Experimental Neuropsychology 12323–339.PubMedCrossRefGoogle Scholar
  11. Jenkins, I. H., Brooks, D. J., Nixon, P. D., Frackowiak, R. S. J. & Passingham, R. E. (1994) Motor sequence learning: A study with positron emission tomography.Journal of Neuroscience 143775–3790.PubMedGoogle Scholar
  12. Jueptner, M., Stephan, K. M., Frith, C. D., Brooks, D. J., Frackowiak, R. S. J. & Passingham, R. E. (1997a) Anatomy of motor learning. I. Frontal cortex and attention to action.Journal of Neurophysiology 771313–1324.Google Scholar
  13. Jueptner, M., Frith, C. D., Brooks, D. J., Frackowiak, R. S. J. & Passingham, R. E. (1997b) Anatomy of motor learning. II. Subcortical structures and learning by trial and error.Journal of Neurophysiology 771325–1337.Google Scholar
  14. Kimura, M., Rajkowski, J. & Evarts, E. V. (1984) Tonically discharging putamen neurons exhibit set dependent responses.Proceedings of the National Academy of Sciences of the United States ofAmerica 814998–5001.CrossRefGoogle Scholar
  15. Kimura, M. (1986) The role of primate putamen neurons in the association of sensory stimuli with movement.Neuroscience Research3, 436–443.PubMedCrossRefGoogle Scholar
  16. Kimura, M., Kato, M. & Shimazaki, H. (1990) Physiological properties of projection neurons in the monkey striatum to the globus pallidus.Experimental Brain Research 82672–676.CrossRefGoogle Scholar
  17. Knopman, D. & Nissen, M. J. (1991) Procedural learning is impaired in Huntington’s disease: Evidence from the serial reaction time task.Neuropsychologia 29245–254.PubMedCrossRefGoogle Scholar
  18. Knowlton, B. J., Mangels, J. A. & Squire, L. R. (1996) A neostriatal habit learning system in humans.Science 2731399–1402.PubMedCrossRefGoogle Scholar
  19. MARSDEN, C. D. (1982) The mysterious motor function of the basal ganglia: the Robert Wartenberg Lecture.Neurology 32514–539.PubMedCrossRefGoogle Scholar
  20. Mishkin, M., Malamut, B. & Bachevalier, J. (1984) Memories and habits: two neural systems. InNeurobiology of Learning and Memory(edited by Lynch, G, McGaugh, J. L. & Weinberger, N. M.) pp. 65–77. New York: Guilford Press.Google Scholar
  21. Ravel, S., Legallet, E. & Apicella, P. (1999) Tonically active neurons in the monkey striatum do not preferentially respond to appetitive stimuli.Experimental Brain Research 128531–534.CrossRefGoogle Scholar
  22. Raz, A., Feingold, A., Zelanskaya, V., Vaadia, E. & Bergman, H. (1996) Neuronal synchronization of tonically active neurons in the striatum of normal and parkinsonian primates.Journal of Neurophysiology 762083–2088.PubMedGoogle Scholar
  23. Saint-Cyr, J. A., Taylor, A. E. & Lang, A. E. (1988) Procedural learning and neostriatal dysfunction in man.Brain 111941–959.PubMedCrossRefGoogle Scholar
  24. Wilson, C. J., Chang, H. T. & Kitai, S. T. (1990) Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum.Journal of Neuroscience 10508–519.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Paul Apicella
    • 1
  • Sabrina Ravel
    • 1
  • Pierangelo Sardo
    • 1
    • 2
  • Eric Legallet
    • 1
  1. 1.Institut de Neurosciences Physiologiques et CognitivesCNRSMarseille cedex 20France
  2. 2.Istituto di Fisiologia UmanaUniversità di PalermoPalermoItaly

Personalised recommendations