Cerebellum lesion impairs eyeblink-like classical conditioning in goldfish

Abstract

The cerebellum of mammals is an essential component of the neural circuitry underlying classical conditioning of eyeblink and other discrete responses. Although the neuroanatomical organization of the cerebellum is notably well conserved in vertebrates, little is actually known about the cerebellar learning functions in nonmammal vertebrate groups. In this work we studied whether the cerebellum of teleost fish plays a critical role in the classical conditioning of a motor response. In Experiment 1, we classically conditioned goldfish in a procedure analogous to the eyeblink conditioning paradigm commonly used in mammals. Goldfish were able to learn to express an eyeblink-like conditioned response to a predictive light (conditioned stimulus) that was paired with a mild electric shock (unconditioned stimulus). The application of unpaired and extinction control procedures demonstrated that also in teleosts the learning of this motor response depends on associative rules. In Experiment 2 we studied whether classical conditioning of this response is critically dependent on the cerebellum and independent of telencephalic structures as occurs in mammals. Cerebellum lesion prevented the acquisition of the eyeblink-like conditioned response whereas telencephalon ablation did not impair the learning of this response. No deficit was observed following lesions in the performance of the unconditioned response or in the percentage of spontaneous responses. These results suggest that cerebellum ablation in goldfish affects a critical component of the circuitry necessary for the acquisition of the conditioned response but does not interfere with the ability of the animal to perform the response itself. The striking similarity in the role of cerebellum in classical conditioning of a motor response between teleost fish and mammals suggests that this learning function of the cerebellum could be a primitive feature of the vertebrate brain that has been conserved through evolution.