Experimental Brain Research

, Volume 110, Issue 1, pp 36–46 | Cite as

Inhibition of the inferior olive during conditioned responses in the decerebrate ferret

  • Germund Hesslow
  • Magnus Ivarsson
Research Article

Abstract

Output from the interpositus nucleus can inhibit the inferior olive, probably via the GABA-ergic nucleo-olivary pathway. It has been suggested that the function of this inhibition might be to regulate synaptic plasticity resulting from parallel fibre/climbing fibre interaction in cerebellar Purkinje cells, by providing negative feedback information to the olive. Thus, when a learned response, generated by the interpositus nucleus, reaches a sufficient amplitude, the olive would be inhibited and further learning blocked. This suggestion was tested in a classical conditioning paradigm. Decerebrate ferrets were trained using electrical skin stimulation of the forelimb as the conditioned stimulus (CS) and periorbital stimulation as the unconditioned stimulus (US). Climbing fibre responses evoked in Purkinje cells by the US were recorded as surface field potentials in the part of the c3 zone controlling eyeblink. It was found that the CS did not inhibit the olive at the beginning of training, but when conditioned responses were large, the olive was inhibited by the CS in some animals. After a number of unpaired CS presentations, which caused extinction of the conditioned response, the inhibition disappeared. The size of individual conditioned responses correlated negatively with the size of the climbing fibre responses evoked by the US. Climbing fibre responses evoked by direct stimulation of the olive were also inhibited. It was concluded that cerebellar output during performance of a conditioned response inhibits the inferior olive. The results thus support the hypothesis of a cerebellar locus of conditioning and are consistent with the proposed role of cerebello-olivary inhibition.

Key words

Cerebellum Classical conditioning Eyeblink Inferior olive Inhibition Ferret 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61Google Scholar
  2. Andersson G (1984) Mutual inhibition between olivary cell groups projecting to different cerebellar microzones in the cat. Exp Brain Res 54:293–303Google Scholar
  3. Andersson G, Hesslow G (1987a) Inferior olive excitability after high frequency climbing fibre activation in the cat. Exp Brain Res 67:523–532Google Scholar
  4. Andersson G, Hesslow G (1987b) Activity of Purkinje cells and interpositus neurones during and after high frequency climbing fibre activation in the cat. Exp Brain Res 67:533–542Google Scholar
  5. Andersson G, Garwicz M, Hesslow G (1988) Evidence for a GABA-mediated inhibition of the inferior olive in the cat. Exp Brain Res 72:450–456Google Scholar
  6. Davis KD, Dostrovsky JO (1986) Modulatory influences of red nucleus stimulation on the somatosensory responses of cat trigeminal subnucleus oralis neurons. Exp Neurol 91:80–101Google Scholar
  7. Gormezano I, Moore JW (1976) Classical conditioning. In: Marx MH (ed) Learning: processes. Macmillan, New York, pp 119–203Google Scholar
  8. Hesslow G (1986) Inhibition of inferior olivary transmission by mesencephalic stimulation in the cat. Neurosci Lett 63:76–80Google Scholar
  9. Hesslow G (1992) Cerebellar inhibition of the inferior olive during conditioned eyeblink responses in decerebrate ferrets. Eur J Neurosci Suppl 5:1063Google Scholar
  10. Hesslow G (1994a) Correspondence between climbing fibre input and motor output in eyeblink related areas in cat cerebellar cortex. J Physiol (Lond) 476:229–244Google Scholar
  11. Hesslow G (1994b) Inhibition of classically conditioned eyeblink responses by stimulation of the cerebellar cortex in the cat. J Physiol (Lond) 476:245–251Google Scholar
  12. Hesslow G (1995) Cerebellum and classical conditioning of eyeblink in decerebrate cats and ferrets. In: Ferrell WR, Proske RU (eds) Neural control of movement. Plenum Press, New York, pp 117–1221Google Scholar
  13. Hesslow G, Ivarsson M (1994) Suppression of cerebellar Purkinje cells during conditioned responses in ferrets. Neuroreport 5:649–652Google Scholar
  14. Hesslow G, Hardiman M, Yeo CH (1990) Cerebellar lesions abolish eyeblink conditioning in the decerebrate rabbit. Eur J Neurosci Suppl 3:301Google Scholar
  15. Ito M (1984) The cerebellum and neuronal control. Raven Press, New YorkGoogle Scholar
  16. Ivarsson M, Hesslow G (1993) Bilateral control of the orbicularis oculi muscle from one cerebellar hemisphere in the ferret. Neuroreport 4:1127–1130CrossRefGoogle Scholar
  17. Kamin L (1969) Predictability, surprise, attention, and conditioning. In: Campbell BA, Church RM (eds) Punishment and aversive behavior. Appleton-Century-Crofts, New York, pp 279–296Google Scholar
  18. Kelly TM, Zuo C-C, Bloedel JR (1990) Classical conditioning of the eyeblink reflex in the decerebrate-decerebellate rabbit. Behav Brain Res 38:7–18Google Scholar
  19. Krupa DJ, Thompson JK, Thompson RF (1993) Localization of a memory trace in the mammalian brain. Science 260:989–991Google Scholar
  20. Mackintosh NJ (1974) The psychology of animal learning. Academic Press, LondonGoogle Scholar
  21. Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437–470Google Scholar
  22. Mauk MD, Thompson RF (1987) Retention of classically conditioned eyelid responses following acute decerebration. Brain Res 403:89–95Google Scholar
  23. McCormick DA, Thompson RF (1984) Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223:296–299Google Scholar
  24. Nelson B, Mugnaini E (1989) Origins of GABA-ergic inputs to the inferior olive. In: Strata P (ed) The olivo-cerebellar system in motor control. (Experimental Brain Research, series 17) Springer, Berlin Heidelberg New York, pp 86–107Google Scholar
  25. Nordholm AF, Lavond DG, Thompson RF (1991) Are eyeblink responses to tone in the decerebrate, decerebellate rabbit conditioned responses? Behav Brain Res 44:27–34Google Scholar
  26. Norman RJ, Villablanca JR, Brown KA, Schwafel JA, Buchwald JS (1974) Classical eyeblink conditioning in the bilaterally hemispherectomized cat. Exp Neurol 44:363–380Google Scholar
  27. Sears LL, Steinmetz JE (1991) Dorsal accessory olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Res 545:114–122Google Scholar
  28. Solomon RL, Turner LH (1962) Discriminative classical conditioning in dogs paralysed by curare can later control discriminative avoidance responses in the normal state. Psychol Rev 69:202–219Google Scholar
  29. Welsh JP, Harvey JA (1989) Cerebellar lesions and the nictitating membrane reflex: performance deficits of the conditioned and unconditioned response. J Neurosci 9:299–311Google Scholar
  30. Welsh JP, Harvey JA (1991) Pavlovian conditioning in the rabbit during inactivation of the interpositus nucleus. J Physiol (Lond) 444:459–480Google Scholar
  31. Yeo CH (1991) Cerebellum and classical conditioning of motor responses. In: Wolpaw JR, Schmidt JT, Vaughan TM (eds) Activity driven CNS changes in learning and development. Ann NY Acad Sci 627:292–304Google Scholar
  32. Yeo CH, Hardiman MJ (1992) Cerebellar cortex and eyeblink conditioning: a reexamination. Exp Brain Res 88:623–638Google Scholar
  33. Yeo CH, Hardiman MJ, Glickstein M (1985a) Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei. Exp Brain Res 60:87–98Google Scholar
  34. Yeo CH, Hardiman MJ, Glickstein M (1985b) Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Exp Brain Res 60:99–113Google Scholar
  35. Yeo CH, Hardiman MJ, Glickstein M (1986) Classical conditioning of the nictitating membrane response of the rabbit. IV. Lesions of the inferior olive. Exp Brain Res 63:81–92Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Germund Hesslow
    • 1
  • Magnus Ivarsson
    • 1
  1. 1.Department of Physiology and BiophysicsLundSweden

Personalised recommendations