Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Selective enhancement of associative learning by microstimulation of the anterior caudate

Nature Neuroscience volume 9, pages 562–568 (2006)Cite this article

Abstract

Primates have the remarkable ability to rapidly adjust or modify associations between visual cues and specific motor responses. Whereas little is known as to how such adjustments in behavioral policy are implemented, recent learning models suggest that the anterior striatum is optimally positioned to have a role in this process. We recorded from single units and delivered microstimulation in the striatum of rhesus monkeys performing an associative learning task. Caudate activity during reinforcement was closely correlated with the rate of learning and peaked during the steepest portion of the learning curve when new associations were being acquired. Moreover, delivering microstimulation in the caudate during the reinforcement period significantly increased the rate of learning without altering the monkeys' ultimate performance. These findings suggest that the caudate is responsible for implementing selective adjustments to the 'associative weights' between sensory cues and motor responses during learning, thus enhancing the likelihood of selecting profitable actions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Single neuronal responses during learning.
Figure 2: Population responses in the caudate during learning.
Figure 3: Locations of all recording sites within the caudate.
Figure 4: Population responses in the putamen during learning.
Figure 5: Effect of microstimulation in the caudate on learning.
Figure 6: Stimulation controls.
Figure 7: Effect of microstimulation in the putamen on learning.

Similar content being viewed by others

References

  1. Alexander, G.E. Basal ganglia-thalamocortical circuits: their role in control of movements. J. Clin. Neurophysiol. 11, 420–431 (1994).

    Article  CAS  Google Scholar 

  2. Flaherty, A.W. & Graybiel, A.M. Input-output organization of the sensorimotor striatum in the squirrel monkey. J. Neurosci. 14, 599–610 (1994).

    Article  CAS  Google Scholar 

  3. Hoover, J.E. & Strick, P.L. Multiple output channels in the basal ganglia. Science 259, 819–821 (1993).

    Article  CAS  Google Scholar 

  4. Houk, J.C., Davis, J.L. & Beiser, D.G. eds. Models of Information Processing in the Basal Ganglia (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  5. McClure, S.M., Laibson, D.I., Loewenstein, G. & Cohen, J.D. Separate neural systems value immediate and delayed monetary rewards. Science 306, 503–507 (2004).

    Article  CAS  Google Scholar 

  6. Pasupathy, A. & Miller, E.K. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature 433, 873–876 (2005).

    Article  CAS  Google Scholar 

  7. Schultz, W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80, 1–27 (1998).

    Article  CAS  Google Scholar 

  8. Fibiger, H.C., LePiane, F.G., Jakubovic, A. & Phillips, A.G. The role of dopamine in intracranial self-stimulation of the ventral tegmental area. J. Neurosci. 7, 3888–3896 (1987).

    Article  CAS  Google Scholar 

  9. Wickens, J.R., Reynolds, J.N. & Hyland, B.I. Neural mechanisms of reward-related motor learning. Curr. Opin. Neurobiol. 13, 685–690 (2003).

    Article  CAS  Google Scholar 

  10. Reynolds, J.N., Hyland, B.I. & Wickens, J.R. A cellular mechanism of reward-related learning. Nature 413, 67–70 (2001).

    Article  CAS  Google Scholar 

  11. O'Doherty, J. et al. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452–454 (2004).

    Article  CAS  Google Scholar 

  12. O'Doherty, J.P. Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr. Opin. Neurobiol. 14, 769–776 (2004).

    Article  CAS  Google Scholar 

  13. Suri, R.E. & Schultz, W. A neural network model with dopamine-like reinforcement signal that learns a spatial delayed response task. Neuroscience 91, 871–890 (1999).

    Article  CAS  Google Scholar 

  14. Smith, A.C. et al. Dynamic analysis of learning in behavioral experiments. J. Neurosci. 24, 447–461 (2004).

    Article  CAS  Google Scholar 

  15. Wirth, S. et al. Single neurons in the monkey hippocampus and learning of new associations. Science 300, 1578–1581 (2003).

    Article  CAS  Google Scholar 

  16. Alexander, G.E. & DeLong, M.R. Microstimulation of the primate neostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties. J. Neurophysiol. 53, 1417–1430 (1985).

    Article  CAS  Google Scholar 

  17. Aosaki, T., Kimura, M. & Graybiel, A.M. Temporal and spatial characteristics of tonically active neurons of the primate's striatum. J. Neurophysiol. 73, 1234–1252 (1995).

    Article  CAS  Google Scholar 

  18. Cohen, M.R. & Newsome, W.T. What electrical microstimulation has revealed about the neural basis of cognition. Curr. Opin. Neurobiol. 14, 169–177 (2004).

    Article  CAS  Google Scholar 

  19. Tehovnik, E.J. Electrical stimulation of neural tissue to evoke behavioral responses. J. Neurosci. Methods 65, 1–17 (1996).

    Article  CAS  Google Scholar 

  20. Hernandez-Lopez, S., Bargas, J., Surmeier, D.J., Reyes, A. & Galarraga, E. D1 receptor activation enhances evoked discharge in neostriatal medium spiny neurons by modulating an L-type Ca2+ conductance. J. Neurosci. 17, 3334–3342 (1997).

    Article  CAS  Google Scholar 

  21. Borland, L.M., Shi, G., Yang, H. & Michael, A.C. Voltammetric study of extracellular dopamine near microdialysis probes acutely implanted in the striatum of the anesthetized rat. J. Neurosci. Methods 146, 149–158 (2005).

    Article  CAS  Google Scholar 

  22. Cragg, S.J., Hille, C.J. & Greenfield, S.A. Dopamine release and uptake dynamics within nonhuman primate striatum in vitro. J. Neurosci. 20, 8209–8217 (2000).

    Article  CAS  Google Scholar 

  23. Hadj-Bouziane, F. & Boussaoud, D. Neuronal activity in the monkey striatum during conditional visuomotor learning. Exp. Brain Res. 153, 190–196 (2003).

    Article  Google Scholar 

  24. Hollerman, J.R., Tremblay, L. & Schultz, W. Influence of reward expectation on behavior-related neuronal activity in primate striatum. J. Neurophysiol. 80, 947–963 (1998).

    Article  CAS  Google Scholar 

  25. Jog, M.S., Kubota, Y., Connolly, C.I., Hillegaart, V. & Graybiel, A.M. Building neural representations of habits. Science 286, 1745–1749 (1999).

    Article  CAS  Google Scholar 

  26. Kawagoe, R., Takikawa, Y. & Hikosaka, O. Expectation of reward modulates cognitive signals in the basal ganglia. Nat. Neurosci. 1, 411–416 (1998).

    Article  CAS  Google Scholar 

  27. Miyachi, S., Hikosaka, O., Miyashita, K., Karadi, Z. & Rand, M.K. Differential roles of monkey striatum in learning of sequential hand movement. Exp. Brain Res. 115, 1–5 (1997).

    Article  CAS  Google Scholar 

  28. Press, W.H., Teukolsky, S.A., Vetterling, W.T. & Flannery, B.P. Numerical Recipes in C++: The Art of Scientific Computing 2nd edn. (Cambridge Univ. Press, Cambridge, UK, 2002).

    Google Scholar 

  29. Schraudolph, N.N. Fast curvature matrix-vector products for second-order gradient descent. Neural Comput. 14, 1723–1738 (2002).

    Article  Google Scholar 

Download references

Acknowledgements

We thank E.N. Brown, W.F. Asaad, J.D. Macklis and R. Amirnovin for their thoughtful comments and critical review of the paper. Funding for this project was provided by the National Institutes of Neurological Disorders and Stroke, the Parkinson Disease Foundation and the Harvard Center for Neurodegeneration and Repair.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, MGH-HMS Center for Nervous System Repair, Massachusetts General Hospital, Harvard Medical School, Boston, 02114, Massachusetts, USA

    Ziv M Williams & Emad N Eskandar

Authors
  1. Ziv M Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emad N Eskandar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emad N Eskandar.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig.1

Paired choice control task. (PDF 626 kb)

Supplementary Methods (PDF 114 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Williams, Z., Eskandar, E. Selective enhancement of associative learning by microstimulation of the anterior caudate. Nat Neurosci 9, 562–568 (2006). https://doi.org/10.1038/nn1662

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1662

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing