Stimulus Contingency and Task Context Encoding within the Anterior Cingulate–Amygdala–Cerebellum Associative Learning Network

Cerebellum (CB) interactions with forebrain systems contribute to learning cognitive and motor tasks, but the nature of these interactions is unknown. Trace eyeblink conditioning (EBC) is an excellent associative learning paradigm for examining interactions between forebrain systems and CB. The anterior cingulate cortex (ACC), central amygdala (AM), and CB are essential for trace EBC, and we previously recorded changes in neuronal activity in these areas during learning with paired presentations of the conditional stimulus (CS) and unconditional stimulus (US). We attributed changes in activity to learning CS–US contingency but did not report contingency manipulations. Here, we analyzed data from the same rats of both sexes during sessions with transitions from CS–US (paired) trials to CS-alone (extinction) trials and from CS-alone trials to CS–US trials. All three areas showed changes in activity with changes in contingency, during both stimuli and the intertrial interval (ITI). Subsets of ACC, AM, and CB neurons showed higher activity during paired trials, while others showed higher activity during extinction trials both during trial events and ITI. Within- and between-area neuronal synchrony and machine learning predictions of behavior from neuronal activity decreased during extinction trials relative to paired trials, indicating widespread effects of contingency change on the ACC–AM–CB network. The findings suggest that the ACC–AM–CB network encodes both within-trial stimulus contingency and between-trial task context. The transition from paired to extinction trials may decrease mossy fiber input consistency to CB from ACC and AM and decrease the likelihood of CRs.