Skip to main content

Self-Stimulation and Synaptic Plasticity

A novel approach to reward-related learning

  • Chapter
  • 176 Accesses

Part of the book series: Advances in Behavioral Biology ((ABBI,volume 52))

Abstract

It has been recognised since the middle of last century that electrical stimulation applied to various brain areas acts as a positive reinforcer. Olds and Milner (1954) were the first to report that rats could learn to press a lever to self-administer electrical current to an electrode implanted in certain brain regions. The discovery of this phenomenon, known as intracranial self-stimulation (ICSS), was a source of excitement amongst psychologists and physiologists alike. In the words of Olds and Milner,1 ICSS was seen as “a methodological foundation for a physiological study of the mechanisms of reward” (pg. 426).

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. J. Olds and P. Milner, Positive reinforcement produced by electrical stimulation of septal and other regions of the rat brain, J. Comp. Physiol. Psych. 47, 419–427 (1954).

    Article  CAS  Google Scholar 

  2. A. C. Catania, Learning (Prentice-Hall Inc., New Jersey, U.S.A, 1979).

    Google Scholar 

  3. W. E. Gibson, L. D. Reid, M. Sakai, and P. B. Porter, Intracranial reinforcement compared with sugar-water reinforcement, Science 148, 1357–1359 (1965).

    Article  PubMed  CAS  Google Scholar 

  4. J. Panksepp and J. A. Trowill, Intraoral self injection: I. Effects of delay reinforcement on resistance to extinction and implications for self-stimulation, Psychon. Sci. 9, 405–406 (1967).

    Google Scholar 

  5. R. J. Beninger, F. Bellisle, and P. M. Milner, Schedule control of behavior reinforced by electrical stimulation of the brain, Science 196(4289), 547–549 (1977).

    Article  PubMed  CAS  Google Scholar 

  6. A. G. Phillips, C. W. Morgan, and G. J. Mogenson, Changes in self-stimulation preference as a function of incentive of alternative rewards, Can. J. Psycho!. 24(4), 289–297 (1970).

    CAS  Google Scholar 

  7. E. S. Valenstein and B. Beer, Reinforcing brain stimulation in competition with water reward and shock avoidance, Science 137, 1052–1054 (1962).

    Article  PubMed  CAS  Google Scholar 

  8. S. Brown and J. A. Trowill, Lever-pressing performance for brain stimulation on F-1 and V-1 schedules in a single-lever situation, Psycho!. Rep. 26(3), 699–706 (1970).

    CAS  Google Scholar 

  9. J. A. Deutsch, Learning and electrical self-stimulation of the brain, J. Theor. Biot 4, 193–214 (1963).

    Article  CAS  Google Scholar 

  10. E. T. Rolls, M. J. Burton, and F. Mora, Neurophysiological analysis of brain-stimulation reward in the monkey, Brain Res. 194(2), 339–357 (1980).

    Article  PubMed  CAS  Google Scholar 

  11. T. J. Crow, A map of the rat mesencephalon for electrical self-stimulation, Brain Res. 36(2), 265–273 (1972).

    Article  PubMed  CAS  Google Scholar 

  12. D. Corbett and R. A. Wise, Intracranial self-stimulation in relation to the ascending dopaminergic systems of the midbrain: a moveable electrode mapping study, Brain Res. 185(1), 1–15 (1980).

    Article  PubMed  CAS  Google Scholar 

  13. R. W. Reynolds, The relationship between stimulation voltage and rate of hypothalamic self-stimulation in the rat, J. Comp. Physiol. Psych. 51, 193–198 (1958).

    Article  CAS  Google Scholar 

  14. A. Ettenberg and C. L. Duvauchelle, Haloperidol blocks the conditioned place preferences induced by rewarding brain stimulation, Behay. Neurosci. 102(5), 687–691 (1988).

    CAS  Google Scholar 

  15. A. Bjorklund and O. Lindvall, in: Handbook of Physiology: the nervous system. Part I, edited by V. B. Mountcastle, F. E. Bloom, and S. R. Geiger (American Physiological Society, Bethesda, 1986), pp. 155–235.

    Google Scholar 

  16. A. Gratton and R. A. Wise, Brain stimulation reward in the lateral hypothalamic medial forebrain bundle: mapping of boundaries and homogeneity, Brain Res. 274(1), 25–30 (1983).

    Article  PubMed  CAS  Google Scholar 

  17. R. M. Beckstead, V. B. Domesick, and W. J. Nauta, Efferent connections of the substantia nigra and ventral tegmental area in the rat, Brain Res. 175(2), 191–217 (1979).

    Article  PubMed  CAS  Google Scholar 

  18. G. Fouriezos and R. A. Wise, Current-distance relation for rewarding brain stimulation, Behay. Brain Res. 14(1), 85–89 (1984).

    CAS  Google Scholar 

  19. J. S. Yeomans, Two substrates for medial forebrain bundle self-stimulation: myelinated axons and dopamine axons, Neurosci. Biobehay. Rev. 13(2–3), 91–98 (1989).

    CAS  Google Scholar 

  20. R. M. Anderson, M. D. Fatigati, and P. P. Rompre, Estimates of the axonal refractory period of midbrain dopamine neurons: their relevance to brain stimulation reward, Brain Res. 718(1–2), 83–88 (1996).

    Article  PubMed  CAS  Google Scholar 

  21. P. Shizgal, C. Bielajew, D. Corbett, R. Skelton, and J. Yeomans, Behavioral methods for inferring anatomical linkage between rewarding brain stimulation sites, J Comp. Physiol. Psych. 94(2), 227–237 (1980).

    Article  CAS  Google Scholar 

  22. R. A. Wise and M. A. Bozarth, Brain reward circuitry: four circuit elements “wired” in apparent series, Brain Res. Bull. 12(2), 203–208 (1984).

    CAS  Google Scholar 

  23. C. Bielajew and P. Shizgal, Evidence implicating descending fibers in self-stimulation of the medial forebrain bundle, J. Neurosci. 6(4), 919–929 (1986).

    PubMed  CAS  Google Scholar 

  24. C. D. Blaha and A. G. Phillips, Application of in vivo electrochemistry to the measurement of changes in dopamine release during intracranial self-stimulation, J. Neurosci. Meth. 34(1–3), 125–133 (1990).

    Article  CAS  Google Scholar 

  25. H. C. Fibiger, F. G. LePiane, A. Jakubovic, and A. G. Phillips, The role of dopamine in intracranial self-stimulation of the ventral tegmental area, J. Neurosci. 7(12), 3888–3896 (1987).

    PubMed  CAS  Google Scholar 

  26. J. A. Stratmann and R. M. Craft, Intracranial self-stimulation in female and male rats: no sex differences using a rate-independent procedure, Drug Alcohol Depend. 46(1–2), 31–40 (1997).

    Article  PubMed  CAS  Google Scholar 

  27. G. E. Hunt, D. M. Atrens, and D. M. Jackson, Reward summation and the effects of dopamine D1 and D2 agonists and antagonists on fixed-interval responding for brain stimulation, Pharmacol. Biochem. Behay. 48(4), 853–862 (1994).

    CAS  Google Scholar 

  28. K. B. Franklin and S N. McCoy, Pimozide-induced extinction in rats: stimulus control of responding rules out motor deficit, Pharmacol. Biochem. Behay. 11(1), 71–75 (1979).

    CAS  Google Scholar 

  29. R. M. Zacharko, S. Zalcman, G. Macneil, M. Andrews, P. D. Mendella, et al., Differential effects of immunologic challenge on self-stimulation from the nucleus accumbens and the substantia nigra, Pharmacol. Biochem. Behay. 58(4), 881–886 (1997).

    CAS  Google Scholar 

  30. J. Moisan and P. P. Rompre, Electrophysiological evidence that a subset of midbrain dopamine neurons integrate the reward signal induced by electrical stimulation of the posterior mesencephalon, Brain Res. 786(1–2), 143–152 (1998).

    Article  PubMed  CAS  Google Scholar 

  31. A. G. Phillips and H. C. Fibiger, in: The neuropharmacological basis of reward, edited by J. M. Liebman and H. C. Fibiger (Oxford Press, Clarendon, 1989), pp. 66–105.

    Google Scholar 

  32. A. G. Phillips, D. A Carter, and H. C. Fibiger, Dopaminergic substrates of intracranial self-stimulation in the caudate-putamen, Brain Res. 104(2), 221–232 (1976).

    Article  PubMed  CAS  Google Scholar 

  33. R. M. Clavier and H. C. Fibiger, On the role of ascending catecholaminergic projections in intracranial self-stimulation of the substantia nigra, Brain Res. 131(2), 271–286 (1977).

    Article  PubMed  CAS  Google Scholar 

  34. B. R. Cooper, R. J. Konkol, and G. R. Breese, Effects of catecholamine depleting drugs and d-amphetamine on self-stimulation of the substantia nigra and locus coeruleus, J. Pharmacol. Exp. Ther. 204(3), 592–605 (1978).

    PubMed  CAS  Google Scholar 

  35. R. A. Wise and P. P. Rompre, Brain dopamine and reward, Annu. Rev. Psycho!. 40, 191–225 (1989).

    Google Scholar 

  36. V. Blanchard, P. Anglade, “ D iewczapolski, M. Savasta, Y. Agid, et al., Dopaminergic sprouting in the rat striatum after partial lesion of the substantia nigra, Brain Res. 709(2), 319–325 (1996).

    Article  PubMed  CAS  Google Scholar 

  37. M. J. Zigmond, E. D Abercrombie, T. W. Berger, A. A. Grace, and E. M. Stricker, Compensations after lesions of central dopaminergic neurons: some clinical and basic implications, Trends Neurosci. 13(7), 290–296 (1990).

    Article  PubMed  CAS  Google Scholar 

  38. A Cherawy, M F Chesselet, R. Romo. V. Levies, and J. Glowinski, Effects of unilateral electrical stimulation of various thalamic nuclei on the release of dopamine from dendrites and nerve terminals of neurons of the two nigrostriatal dopaminergic pathways, Neuroscience 8(4), 767–780 (1983).

    Article  Google Scholar 

  39. M. A. Castellano and M. Rodriguez Diaz, Nigrostriatal dopaminergic cell activity is under control by substantia nigra of the contralateral brain side: electrophysiological evidence, Brain Res. Bull. 27(2), 213–218 (1991).

    Article  PubMed  CAS  Google Scholar 

  40. Y. Masuo and I. Kanazawa, Effects of the unilateral striatal lesion on neurotransmitter markers in the contralateral striatum and both substantia nigrae of the rat, Neuroscience 27(3), 827–836 (1988).

    Article  PubMed  CAS  Google Scholar 

  41. J. H. Fallon, C. Wang, Y. Kim, N. Canepa, S. Loughlin, et al., Dopamine-and cholecystokinin-containing neurons of the crossed mesostriatal projection, Neurosci. Lett. 40(3), 233–238 (1983).

    CAS  Google Scholar 

  42. R. J. Beninger and R. Ranaldi, Microinjections of flupenthixol into the caudate-putamen but not the nucleus accumbens, amygdala or frontal cortex of rats produce intra-session declines in food-rewarded operant responding, Behav Brain Res. 55(2).203–212 (1993).

    Article  PubMed  CAS  Google Scholar 

  43. T. Aosaki, A. M. Graybiel, and M. Kimura, Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys, Science 265(5170), 412–415 (1994).

    Article  PubMed  CAS  Google Scholar 

  44. M. R. Kilpatrick, M. B. Rooney, D. J. Michael, and R. M. Wightman, Extracellular dopamine dynamics in rat caudate-putamen during experimenter-delivered and intracranial self-stimulation, Neuroscience 96(4), 697–706 (2000).

    Article  PubMed  CAS  Google Scholar 

  45. P. A. Garns, M. Kilpatrick, M. A. Bunin, D. Michael, Q. D. Walker, et al., Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation, Nature 398(6722), 67–69 (1999).

    Article  Google Scholar 

  46. R. Major and N. White, Memory facilitation by self-stimulation reinforcement mediated by the nigroneostriatal bundle, Physiol. Behay. 20(6), 723–733 (1978).

    Article  CAS  Google Scholar 

  47. N. White and R. Major, Effect of pimozide on the improvement in learning produced by self-stimulation and by water reinforcement, Pharmacol. Biochem. Behay. 8(5), 565–571 (1978).

    CAS  Google Scholar 

  48. A. Routtenberg and N. Holzman, Memory disruption by electrical stimulation of substantia nigra, pars compacta, Science 181(94), 83–86 (1973)

    Article  PubMed  CAS  Google Scholar 

  49. H. C. Fibiger and A. G. Phillips, Retrograde amnesia after electrical stimulation of the substantia nigra: mediation by the dopaminergic nigroneostriatal bundle, Brain Res. 116(1), 23–33 (1976).

    Article  PubMed  CAS  Google Scholar 

  50. J. Wickens and R. Kotter, in: Models of information processing in the basal ganglia, edited by J. C. Houk, J. L. Davis, and D. G. Beiser (M.LT.Press, Cambridge MA, 1995), pp. 187–214.

    Google Scholar 

  51. A. D. Smith and J P. Bolam, The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones, Trends Neurosci. 13(7), 259–265 (1990).

    Article  PubMed  CAS  Google Scholar 

  52. H. Kita, Glutamatergic and GABAergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations, Neuroscience 70(4), 925–940 (1996).

    Article  PubMed  CAS  Google Scholar 

  53. Z. G. Jiang and R. A. North, Membrane properties and synaptic responses of rat striatal neurones in vitro, J. Physiol. 443, 533–553 (1991).

    PubMed  CAS  Google Scholar 

  54. F. Gonon, Prolonged and extrasynaptic excitatory action of dopamine mediated by DI receptors in the rat striatum in vivo, J. Neurosci. 17(15), 5972–5978 (1997).

    PubMed  CAS  Google Scholar 

  55. G. V. Williams and J. Millar, Concentration-dependent actions of stimulated dopamine release on neuronal activity in rat striatum, Neuroscience 39(1), 1–16 (1990).

    Article  PubMed  CAS  Google Scholar 

  56. M. S. Levine, Z. Li, C. Cepeda, H. C. Cromwell, and K. L. Altemus, Neuromodulatory actions of dopamine on synaptically-evoked neostriatal responses in slices, Synapse 24(1), 65–78 (1996).

    Article  PubMed  CAS  Google Scholar 

  57. T. V. Bliss and G. L. Collingridge, A synaptic model of memory: long-term potentiation in the hippocampus, Nature 361(6407), 31–39 (1993).

    Article  PubMed  CAS  Google Scholar 

  58. K. Tang, M. J. Low, D. K. Grandy, and D. M. Lovinger, Dopamine-dependent synaptic plasticity in striatum during in vivo development, Proc. Natl. Acad. Sci. U. S. A. 98(3), 1255–1260. (2001).

    Article  PubMed  CAS  Google Scholar 

  59. P. Calabresi, R. Maj, N. B. Mercuri, and G. Bernardi, Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum, Neurosci. Lett. 142(1), 95–99 (1992).

    CAS  Google Scholar 

  60. J. R. Wickens, A. J. Begg, and G. W. Arbuthnott, Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex in vitro, Neuroscience 70(1), 1–5 (1996).

    Article  PubMed  CAS  Google Scholar 

  61. J. N. Kerr and J. R. Wickens, Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro, J. Neurophysiol. 85(1), 117–124 (2001).

    PubMed  CAS  Google Scholar 

  62. P. Calabresi, P. Gubellini, D. Centonze, B. Picconi, G. Bernardi, et al., Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity, J. Neurosci. 20(22), 8443–8451 (2000).

    PubMed  CAS  Google Scholar 

  63. L. Nowak, P. Bregestovski, P. Ascher, A. Herbet, and A. Prochiantz, Magnesium gates glutamate-activated channels in mouse central neurones, Nature 307(5950), 462–465 (1984).

    Article  PubMed  CAS  Google Scholar 

  64. M. O. Krebs, J. M. Desce, M. L. Kernel, C. Gauchy, G. Godeheu, et al., Glutamatergic control of dopamine release in the rat striatum: evidence for presynaptic N-methyl-D-aspartate receptors on dopaminergic nerve terminals, J. Neurochem. 56(1), 81–85 (1991).

    Article  PubMed  CAS  Google Scholar 

  65. S. Jin and B. B. Fredholm, Electrically-evoked dopamine and acetylcholine release from rat striatal slices perfused without magnesium: regulation by glutamate acting on NMDA receptors, Br. J. Pharmacol. 121(7), 1269–1276 (1997).

    Article  PubMed  CAS  Google Scholar 

  66. M. Ochi, H. Inoue, S. Koizumi, S. Shibata, and S. Watanabe, Long-term enhancement of dopamine release by high frequency tetanic stimulation via a N-methyl-D-aspartate-receptor-mediated pathway in rat striatum, Neuroscience 66(1), 29–36 (1995).

    Article  PubMed  CAS  Google Scholar 

  67. P. Calabresi, E. Fedele, A. Pisani, G. Fontana, N. B. Mercuri, et al., Transmitter release associated with long-term synaptic depression in rat corticostriatal slices, Eur. J. Neurosci. 7(9), 1889–1894 (1995).

    Article  PubMed  CAS  Google Scholar 

  68. J. N. J. Reynolds and J. R. Wickens, Substantia nigra dopamine regulates synaptic plasticity and membrane potential fluctuations in the rat neostriatum, in vivo, Neuroscience 99(2), 199–203 (2000).

    Article  PubMed  CAS  Google Scholar 

  69. A. A. Grace and B. S. Bunney, The control of firing pattern in nigral dopamine neurons: burst firing, J. Neurosci. 4(1 I), 2877–2890 (1984).

    PubMed  CAS  Google Scholar 

  70. J. N. J. Reynolds, B. I. Hyland, and J. R. Wickens, A cellular mechanism of reward-related learning, Nature 413(6851), 67–70 (2001).

    Article  PubMed  CAS  Google Scholar 

  71. C. J. Wilson and Y. Kawaguchi, The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons, J. Neurosci. 16(7), 2397–2410 (1996).

    PubMed  CAS  Google Scholar 

  72. G. E. Alexander and M. D. Crutcher, Preparation for movement: neural representations of intended direction in three motor areas of the monkey, J. Neurophysiol. 64(1), 133–150 (1990).

    PubMed  CAS  Google Scholar 

  73. M. Kimura, Behaviorally contingent property of movement-related activity of the primate putamen, J. Neurophysiol. 63(6), 1277–1296 (1990).

    PubMed  CAS  Google Scholar 

  74. K. J. Jeffery and R. G. Morris, Cumulative long-term potentiation in the rat dentate gyms correlates with, but does not modify, performance in the water maze, Hippocampus 3(2), 133–140 (1993).

    Article  PubMed  CAS  Google Scholar 

  75. J. P. Walsh and R. Dunia, Synaptic activation of N-methyl-D-aspartate receptors induces short-term potentiation at excitatory synapses in the striatum of the rat, Neuroscience 57(2), 241–248 (1993).

    Article  PubMed  CAS  Google Scholar 

  76. E. L. Thomdike, A proof of the law of effect, Science 77(1989), 173–175 (1933).

    Article  Google Scholar 

  77. T. W. Robbins and B. J. Everitt, Neurobehavioural mechanisms of reward and motivation, Curr. Opin. Neurobiol. 6(2), 228–236 (1996).

    Article  PubMed  CAS  Google Scholar 

  78. S. B. Floresco, C. D. Blaha, C. R. Yang, and A. G. Phillips, Dopamine D1 and NMDA receptors mediate potentiation of basolateral amygdala-evoked firing of nucleus accumbens neurons, J Neurosci. 21(16), 6370–6376 (2001).

    PubMed  CAS  Google Scholar 

  79. J. Wickens, B. Hyland, and G. Anson, Cortical cell assemblies: a possible mechanism for motor programs, J. Motor Behay. 26(2), 66–82 (1994).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer Science+Business Media New York

About this chapter

Cite this chapter

Reynolds, J.N.J., Wickens, J.R. (2002). Self-Stimulation and Synaptic Plasticity. In: Nicholson, L.F.B., Faull, R.L.M. (eds) The Basal Ganglia VII. Advances in Behavioral Biology, vol 52. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0715-4_30

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-0715-4_30

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5207-5

  • Online ISBN: 978-1-4615-0715-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics