Bilateral electrolytic lesions of the anteroventral (AV) nucleus of the thalamus given after training impaired retention performance (extinction and reacquisition) of rabbits in a differential avoidance conditioning task. In addition, the lesions abolished the excitatory, discriminative multiple-unit discharges that had developed in the cingulate and retrosplenial cortices to the auditory conditional stimuli (CSs) during the course of behavioral acquisition, prior to the induction of the lesions. The excitatory discharges were supplanted in the subjects with lesions by CS-elicited reduction of neuronal firing to levels below the prestimulus baseline. Lesions given before training did not disrupt behavioral acquisition, but they did eliminate the excitatory tone-elicited neuronal discharges that normally occur in the cortex before and during training. The CS-elicited reduction of neuronal firing did not occur at the beginning of training in the subjects given lesions before training, but it developed during the course of training. The lesions did not eliminate the excitatory and discriminative neuronal activity of the prefrontal cortex. These results demonstrate that excitatory and discriminative neuronal discharges in the cingulate and retrosplenial cortices are critically dependent on the connections of these areas with the anterior thalamic nuclei. Also the lesion-induced disruption of performance during extinction and reacquisition but not during original learning confirms a prediction from past electrophysiological studies, that the AV thalamic nucleus is involved in the mediation of the maintenance and retention of the conditioned avoidance behavior, but not in its original acquisition.