Douchamps, V. | bioRxiv Science

bioRxiv2024

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) with hippocampal rhythms in male rats acquiring and switching between spatial and visual discrimination tasks in a Y-maze. ACC population and single unit activity responded 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 detection of contingency changes for cognitive flexibility, a function that is attenuated after it is damaged.

neuroscience↗

bioRxiv2022

Hippocampal gamma oscillations form complex ensembles modulated by behavior and learning

The hippocampus and the entorhinal cortex display a rich oscillatory activity, believed to support neural information processing in key cognitive functions1. In the hippocampal region CA1, a "slow gamma" rhythm (30-80 Hz) generated in CA3 would support memory retrieval whereas a "medium gamma" rhythm (60-120 Hz) generated in the entorhinal cortex would support memory encoding2,3. However, descriptions involving discrete gamma sub-bands can only partially account for the haphazard diversity of oscillatory behaviors observed in individual recordings during spatial navigation behavior. Here, we stress that transient gamma oscillatory episodes at any frequency or phase relative to the ongoing theta (4-12 Hz) rhythm can be recorded at any layer within CA1. Eventually, the commonly reported averages are dominated by a minority of very strong power events overshadowing gamma heterogeneity. Nevertheless, we show that such gamma diversity can be naturally explained by a simple mechanistic model, and that behavior-related information (position within a maze) can be decoded from most individual gamma events, despite their low power and erratic-like nature. Our results indicate that behavior specifically shapes ensembles of irregular hippocampal gamma oscillations, in a way which evolves with learning, depends on the hippocampal layer and is hard to reconcile with the hypothesis of rigid, narrowly tuned gamma sub-bands. Beyond randomness, the pervasive gamma diversity may thus reflect complexity at the "fringe-of-synchrony"4 likely functional but invisible to classic average-based analyses.

neuroscience↗