Abstract

Minimizing errors is an important aspect of learning. However, it is not enough merely to record if an error occurred. For efficient learning, information about the magnitude of errors is critical. Did my tennis swing completely miss the target or did I hit the ball, but not quite in the sweet spot? How can neurons - which have traditionally been thought of as binary units - signal the magnitude of an error? Here I review evidence that eyeblink conditioning - a basic form of motor learning - depends on graded signals from the inferior olive which guides plasticity in the cerebellum and ultimately tunes behavior. Specifically, evidence suggests that: (1) Error signals are conveyed to the cerebellum via the inferior olive; (2) Signals from the inferior olive are graded; (3) The strength of the olivary signal affects learning; (4) Cerebellar feedback influences the strength of the olivary signal. I end the review by exploring how graded error signals might explain some behavioral learning phenomena.

Highlights

  • Eyeblink conditioning depends on the cerebellumA subject who is presented with a tone followed by a corneal air-puff will, after some repetitions, begin to blink in response to the tone

  • Minimizing errors is an important aspect of learning

  • This might seems like a sensible strategy, but if it is treated as an imperative, organisms would soon be unable to do anything because, just like a Raindance is sometimes followed by rain, all stimuli and behaviors are sometimes followed by pain

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Summary

Eyeblink conditioning depends on the cerebellum

A subject who is presented with a tone followed by a corneal air-puff will, after some repetitions, begin to blink in response to the tone. In more formal terms: repeatedly pairing a neutral conditional stimulus (CS), with a blink-eliciting unconditional stimulus (US), will lead to the subject producing a conditional blink response (CR) to the tone CS (Hilgard & Campbell, 1936; Kehoe, 1983b; Moore, 2002). Eyeblink conditioning is dependent on the cerebellum We know this based on evidence from lesioning studies (McCormick & Thompson, 1984; Yeo, Hardiman, & Glickstein, 1984, 1985a, 1985b), pharmacological studies (Hardiman, Ramnani, & Yeo, 1996), neurophysiological studies We know this based on evidence from lesioning studies (McCormick & Thompson, 1984; Yeo, Hardiman, & Glickstein, 1984, 1985a, 1985b), pharmacological studies (Hardiman, Ramnani, & Yeo, 1996), neurophysiological studies (Halverson, Khilkevich, & Mauk, 2015; Hesslow, 1994a; Jirenhed, Bengtsson, & Hesslow, 2007 Chap. 45; Ten Brinke et al, 2015), optogenetic studies (Heiney, Kim, Augustine, & Medina, 2014), and patient studies (Gerwig et al, 2005; Gerwig, Kolb, & Timmann, 2007; Wu et al, 2018)

Neural mechanisms
CS and US pathways
Climbing fibers and complex spikes
The inferior olive regulates firing in Purkinje cells
The inferior olive convey error messages
The olive fires in bursts
The shape of complex spikes
The nucleo-olivary pathway
Closing the loop
Learning correlates with the strength of the olivary signal
Changing the direction of learning experimentally
The Rescorla-Wagner model
Kamin blocking
Overshadowing
Experimental predictions
Predictions
A Purkinje cell pause reduce the number of spikes in a climbing fiber burst
Findings
Conclusion

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