Rat anterior cingulate neurons responsive to rule or strategy changes are modulated by the hippocampal theta rhythm and sharp‐wave ripples

To better understand neural processing during adaptive learning of stimulus‐response‐reward contingencies, we recorded synchrony of neuronal activity in anterior cingulate cortex (ACC) and hippocampal rhythms in male rats acquiring and switching between spatial and visual discrimination tasks in a Y‐maze. ACC population activity as well as single unit activity shifted shortly after task rule changes or just before the rats adopted different task strategies. Hippocampal theta oscillations (associated with memory encoding) modulated an elevated proportion of rule‐change responsive neurons (70%), but other neurons that were correlated with strategy‐change, strategy value and reward‐rate were not. However, hippocampal sharp wave‐ripples modulated significantly higher proportions of rule‐change, strategy‐change and reward‐rate responsive cells during post‐session sleep but not pre‐session sleep. This suggests an underestimated mechanism for hippocampal mismatch and contextual signals to facilitate ACC to detect contingency changes for cognitive flexibility, a function that is attenuated after it is damaged. Rats were trained in binary choice spatial (go‐left and go‐right rules) and visual discrimination (lit arm/unlit arm) tasks. Task contingencies changed after criterion performance was reached. Anterior cingulate neurons could increase or decrease firing rates after rule changes (RC neurons) and/or prior to behavioural strategy/policy changes (SC neurons). Rule change (RC) neurons were modulated by the hippocampal (HPC) theta rhythm. Both RC and SC neurons were modulated by HPC sharp wave‐ripples.