Eye Blink Conditioning

Eye-blink conditioning is perhaps the best studied model system for examining the neural basis of sensorimotor learning in mammals. In this form of Pavlovian conditioning, a neutral stimulus such as a tone is repeatedly paired with an aversive stimulus such as an airpuff to the eye. The airpuff is an unconditioned stimulus (US): It automatically elicits an unconditioned response (UR), either a blink in humans or the extension of a protective membrane in rabbits. Initially, the tone, or conditioned stimulus (CS), causes no response. However, after training, the animal produces a conditioned response (CR) following the tone. The CR is timed to occur just prior to the onset of the US, and in this way it is adaptive as it attenuates the aversive consequences of the US. The order and timing of the CS-US events are critical. The tone must precede the airpuff (i.e., be predictive of the US). Also, the two events must be separated by a fixed interval or small set of fixed intervals. Training is poor or absent if the interval between the CS and US is random.

Despite the fact that eye-blink conditioning requires only extremely simple movements, the task contains some basic ingredients of motor learning: First, the appropriate response, the blink, must have no previous associations with the critical stimulus (e.g., the tone). Second, the characteristics of the response are critical for evaluating performance. If the blink is not timed correctly, then it will be of no benefit. For example, the blink is not adaptive if it occurs immediately upon presentation of the tone or if the air puff will not occur for another 500 msec. Thus, the behavior must be refined with practice so that the motor commands are precisely coordinated with environmental events. Finally, it appears that learning for this task is largely implicit. Individuals with anterograde amnesia are able to learn during eye-blink conditioning, at least under certain conditions.

Richard Thompson and colleagues have established the involvement of the cerebellum in eye-blink conditioning. Lesions of the cerebellum can abolish the CR in animals that have undergone conditioning and prevent the acquisition of the CR in a naive animal.

Importantly, the UR remains largely intact, indicating that the deficit is not one of motor production but specifically related to learning. Although most work has been done on the rabbit, the relationship between cerebellar pathology and eye-blink conditioning has been observed in a range of species including humans.

Lesion and physiological methods have been used to identify the component pathways supporting eye-blink conditioning within the cerebellum. When the tone is replaced by stimulation to the mossy fibers, eye-blink conditioning proceeds normally, indicating that parallel fibers represent the CS. Similarly, when the US is replaced by stimulation to the climbing fibers, conditioning is also normal. Thus, the two input pathways to the cerebellum convey representations of the CS and US. The locus at which an association is formed between the CS and US (i.e., the site of learning) has been a subject of considerable debate. One possibility is the primary site of convergence of these inputs—the Purkinje cells of the cerebellar cortex. Another possibility is the deep cerebellar nuclei given that both the mossy and climbing fibers send collaterals to the nuclei. Indeed, lesions of the nuclei completely abolish the CR, whereas lesions of the cerebellar cortex disrupt the timing of the CR. It thus appears that the association of the CS and US can occur at multiple levels. For the CR to be acquired, the cerebellar nuclei must be intact; for the response to be appropriately timed and thus adaptive, the cerebellar cortex is required.

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