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Simple and Complex Spike Firing Patterns in Purkinje Cells During Classical Conditioning

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Abstract

Classical blink conditioning is known to depend critically on the cerebellum and the relevant circuitry is gradually being unravelled. Several lines of evidence support the theory that the conditioned stimulus is transmitted by mossy fibers to the cerebellar cortex whereas the unconditioned stimulus is transmitted by climbing fibers. This view has been dramatically confirmed by recent Purkinje cell recordings during training with a classical conditioning paradigm. We have tracked the activity of single Purkinje cells with microelectrodes for several hours in decerebrate ferrets during learning, extinction, and relearning. Paired peripheral forelimb and periocular stimulation, as well as paired direct stimulation of cerebellar afferent pathways (mossy and climbing fibers) causes acquisition of a pause response in Purkinje cell simple spike firing. This conditioned Purkinje cell response has temporal properties that match those of the behavioral response. Its latency varies with the interstimulus interval and it responds to manipulations of the conditioned stimulus in the same way that the blink does. Complex spike firing largely mirrors the simple spike behavior. We have previously suggested that cerebellar learning is subject to a negative feedback control via the inhibitory nucleo-olivary pathway. As the Purkinje cell learns to respond to the conditioned stimulus with a suppression of simple spikes, disinhibition of anterior interpositus neurons would be expected to cause inhibition of the inferior olive. Observations of complex spike firing in the Purkinje cells during conditioning and extinction confirm this prediction. Before training, complex spikes are unaffected or facilitated by the conditioned stimulus, but as the simple spike pause response develops, spontaneous and stimulus-evoked complex spikes are also strongly suppressed by the conditioned stimulus. After extinction of the simple spike pause response, the complex spikes reappear.

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References

  1. McCormick DA, Thompson RF (1984) Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223(4633):296–299. (Jan 20)

    Article  PubMed  CAS  Google Scholar 

  2. Yeo CH, Hardiman MJ, Glickstein M (1985) Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei. Exp Brain Res 60(1):87–98

    PubMed  CAS  Google Scholar 

  3. Yeo CH, Hardiman MJ, Glickstein M (1985) Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Exp Brain Res 60(1):99–113

    PubMed  CAS  Google Scholar 

  4. Hesslow G, Yeo CH (2002) The functional anatomy of skeletal conditioning. In: Moore JW (ed) A neuroscientist’s guide to classical conditioning. Springer, New York, pp 86–146

    Google Scholar 

  5. Yeo CH, Hesslow G (1998) Cerebellum and conditioned reflexes. Trends Cogn Sci 2(9):322–330. (Sept)

    Article  Google Scholar 

  6. Christian KM, Thompson RF (2005) Long-term storage of an associative memory trace in the cerebellum. Behav Neurosci 119:526–537

    Article  PubMed  Google Scholar 

  7. Albus J (1971) A theory of cerebellar function. Math Biosci 10:25–61

    Article  Google Scholar 

  8. Yeo CH, Hardiman MJ, Glickstein M (1985) Classical conditioning of the nictitating membrane response of the rabbit. III. Connections of cerebellar lobule HVI. Exp Brain Res 60(1):114–126

    Article  PubMed  CAS  Google Scholar 

  9. Bengtsson F, Hesslow G (2006) Cerebellar control of the inferior olive. Cerebellum 5:7–14

    Article  PubMed  CAS  Google Scholar 

  10. Montarolo PG, Palestini M, Strata P (1982) The inhibitory effect of the olivocerebellar input on the cerebellar Purkinje cells in the rat. J Physiol (Lond) 332:187–202. (Nov)

    CAS  Google Scholar 

  11. Colin F, Desclin J, Manil J (1979) Quantitative relationship between simple spike firing pattern and evoked complex spikes of cerebellar Purkinje cells after acute chemical destruction of the inferior olive [proceedings]. J Physiol 295:62P–63P. (Oct)

    PubMed  CAS  Google Scholar 

  12. Mauk MD, Steinmetz JE, Thompson RF (1986) Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc Natl Acad Sci U S A 83(14):5349–5353. (July)

    Article  PubMed  CAS  Google Scholar 

  13. Hesslow G (1994) Correspondence between climbing fibre input and motor output in eyeblink-related areas in cat cerebellar cortex. J Physiol (Lond) 476(2):229–244. (Apr 15)

    CAS  Google Scholar 

  14. Hesslow G (1994) Inhibition of classically conditioned eyeblink responses by stimulation of the cerebellar cortex in the decerebrate cat. J Physiol (Lond) 476(2):245–256. (Apr 15)

    CAS  Google Scholar 

  15. Jirenhed DA, Bengtsson F, Hesslow G (2007) Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. J Neurosci 27(10):2493–2502. (Mar 7)

    Article  PubMed  CAS  Google Scholar 

  16. Andersson G, Garwicz M, Hesslow G (1988) Evidence for a GABA-mediated cerebellar inhibition of the inferior olive in the cat. Exp Brain Res 72(3):450–456

    Article  PubMed  CAS  Google Scholar 

  17. Bengtsson F, Jirenhed D-A, Hesslow G (2007) Extinction of conditioned blink responses by cerebello-olivary stimulation. Neuroreport 18(14):1479–1482

    Article  PubMed  Google Scholar 

  18. Kamin LJ (1969) Predictability, surprise attention and conditioning. In: Campbell B, Church R (eds) Punishment and aversive behavior. Appleton-Century-Crofts, New York

    Google Scholar 

  19. Marchant HG, Moore JW (1993) Blocking of the rabbit’s conditioned nictitating membrane response in Kamin’s two-stage paradigm. J Exp Psychol 101(1):155–158. (Nov)

    Article  Google Scholar 

  20. Kehoe EJ, White NE (2004) Overexpectation: response loss during sustained stimulus compounding in the rabbit nictitating membrane preparation. Learn Memory 11:476–483

    Article  Google Scholar 

  21. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and non reinforcement. In: Black AH, Prokasy WF (eds) Classical conditioning II. Appleton-Century-Crofts, New York, pp 64–99

    Google Scholar 

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Acknowledgements

This work was supported by the Swedish Research Council (no. 09899) and the Segerfalk, Söderberg and Åhlen foundations.

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Correspondence to Germund Hesslow.

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Rasmussen, A., Jirenhed, DA. & Hesslow, G. Simple and Complex Spike Firing Patterns in Purkinje Cells During Classical Conditioning. Cerebellum 7, 563–566 (2008). https://doi.org/10.1007/s12311-008-0068-2

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