Simple and Complex Spike Firing Patterns in Purkinje Cells During Classical Conditioning
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.
KeywordsSimple spike firing Complex spike firing Purkinje cells Classical conditioning Cerebellum
This work was supported by the Swedish Research Council (no. 09899) and the Segerfalk, Söderberg and Åhlen foundations.
- 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 86–146Google 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)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)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)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 YorkGoogle 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 64–99Google Scholar