Single-unit evidence for eye-blink conditioning in cerebellar cortex is altered, but not eliminated, by interpositus nucleus lesions

Abstract

Many theories of motor learning explain learning-related changes in motor behavior in terms of plasticity in the cerebellar cortex. Empirical evidence, however, does not always appear to be consistent with such formulations. It is the anterior cerebellar interpositus nucleus (aINP) that seems to be essential for acquisition and retention of conditioned eye-blink responses under most circumstances and it has been therefore suggested that the aINP is the critical site of learning-related plasticity during eye-blink conditioning. Supporting this conclusion are studies demonstrating that multiple-unit conditioning-related neural activity patterns observed in many brain regions disappear after aINP lesion. The possibility that the cerebellar cortex may be involved in forming these patterns has not been assessed adequately, however. In the current study, trained rabbits received kainic acid lesions of the INP. After recovery, the animals underwent additional sessions of conditioning during which single-unit activity was recorded from the cerebellar cortex. Our results suggest that the aINP is not the sole site of plasticity during eye-blink conditioning, as a subset of the neurons recorded from lesioned animals demonstrated conditioning-related firing patterns. The lesions did change the character of these firing patterns from those observed in saline controls, however, in ways that can be generally described as a loss of organization. The normal tendency for the population of cortical cells to change firing rate together, for instance, was significantly less noticeable in lesioned animals. These results suggest that the aINP may be involved in the production of important features of conditioned responding, such as system timing function, therefore suggesting the need for more models that incorporate aINP and brain stem feedback as integral to the production of organized neural and behavioral responses.