Multiunit activity of cingulate cortex and the anterior ventral (AV) thalamic nucleus was recorded as rabbits learned to avoid a shock by locomoting in response to a tone (CS+) and to ignore a nonpredictive tone (CS-). Rabbits with anterior dorsal (AD) thalamic lesions avoided shock more often than controls during the first training session and the first session of extinction training given after the completion of acquisition. Training-induced neuronal changes in cingulate cortex and in components of the AV nucleus were lost in the rabbits with lesions. These effects were comparable to previously observed effects of subicular lesions. It is proposed that interactions of AD thalamic, subicular, and cingulate cortical neurons yield a stable mnemonic representation of the associative significance of the CS. The representation is used in a comparator circuit, which inhibits behavior when unexpected events occur.