Changes of cingulothalamic topographic excitation patterns and avoidance response incubation over time following initial discriminative conditioning in rabbits

Abstract

Neurons in particular layers of cingulate cortex and in limbic thalamic nuclei exhibit peak firing rates in response to a positive conditional stimulus (CS+) in particular stages of discriminative learning. A given area is maximally activated by the CS+ in the initial, an intermediate, or a late stage of behavioral acquisition, and activation in all of the areas diminishes as training continues after the peak of activation occurs. Thus, the topographic distribution of activation in these areas depends on the stage of behavioral acquisition. The present study determined whether the acquisition-related changes of the topographic distributions of peak firing rates in CS-elicited activity are driven exclusively by the repetition of conditioning trials (i.e., practice) or may occur as well with the passage of time, similar to putative processes of memory consolidation. Multiunit activity was recorded in cingulate cortex and in the anterior dorsal (AD), anterior ventral (AV), and medial dorsal (MD) thalamic nuclei as rabbits learned to step in response to a warning tone (CS+) to prevent a scheduled foot-shock, and to ignore a different tone (CS-) not predictive of foot-shock. The rabbits received two training sessions, S1 and S2. S2 followed S1 immediately in one group of rabbits and after 48 h in a different group. Significant neuronal discharge increments occurred from S1 to S2 in the 48-h group but not in the 0-h group, for the areas (posterior cingulate cortex, AV thalamic nucleus) that previously showed only late-stage activation. Significant discharge increments occurred from S1 to S2 in the 0-h group but not in the 48-h group in areas (anterior cingulate cortex, the AD, and MD thalamic nuclei) that previously exhibited early stage activation. These results indicate that the trial-driven topographic distribution changes also occur with the passage of time after limited initial training. It is suggested that the trial-driven and time-related changes may have a common functional relevance concerning memory consolidation.