Learning-related activation in the auditory system of the rat produced by long-term habituation: a 2-deoxyglucose study

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Autoradiography with [ 14C]2-deoxyglucose (2-DG) was used to examine the functional activity of the rat auditory system during long- and short-term habituation of the acoustic startle reflex. The data showed that presentation of the acoustic stimulus to long-term habituated rats resulted in a learning-related metabolic enhancement that was significantly greater than the response evoked by the same acoustic stimulus in the inexperienced rats. This enhancement was localized to brainstem and midbrain auditory nuclei and no significant changes occurred at thalamocortical levels of the auditory pathway. The largest difference in 2-DG uptake between long- and short-term habituated rats was in the lateral superior olivary nucleus (LSO). The LSO activation suggests that olivocochlear efferents may operate in a central feedback control of peripheral auditory input during long-term habituation. Findings of enhanced metabolism from the cochlear nuclei to the central nucleus of the inferior colliculus indicated that active processes of neuronal plasticity take place in the lower auditory system during long-term habituation. The results provide the first demonstration of how a nonassociative learning experience such as long-term habituation modifies the metabolic activity of the auditory system. The findings support the conclusion that auditory responses of behaving animals to acoustic stimuli are dependent not only on the physical parameters of a stimulus, but also on its learned behavioral significance.