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Short-term memory enables incorporation of recent experience into subsequent decision-making. This processing recruits both the prefrontal cortex and hippocampus, where neurons encode task cues, rules, and outcomes. However, precisely which information is carried when, and by which neurons, remains unclear. Using population decoding of activity in rat medial prefrontal cortex (mPFC) and dorsal hippocampal CA1, we confirm that mPFC populations lead in maintaining sample information across delays of an operant non-match to sample task, despite individual neurons firing only transiently. During sample encoding, distinct mPFC subpopulations joined distributed CA1-mPFC cell assemblies hallmarked by 4–5 Hz rhythmic modulation; CA1-mPFC assemblies re-emerged during choice episodes but were not 4–5 Hz modulated. Delay-dependent errors arose when attenuated rhythmic assembly activity heralded collapse of sustained mPFC encoding. Our results map component processes of memory-guided decisions onto heterogeneous CA1-mPFC subpopulations and the dynamics of physiologically distinct, distributed cell assemblies. [Display omitted] • Hippocampal-cortical (CA1-PFC) activity reconfigures during different memory stages • Distributed CA1-PFC assemblies co-fire with 5 Hz rhythmicity during memory loading • Tiled activation in PFC maintains memory across delay periods • Collapse of rhythmic CA1-PFC assemblies heralds unstable delay coding and errors Domanski, Kucewicz, et al. uncover neurophysiological mechanisms that support progression through encoding, maintenance, and recall of memory. Their findings reconcile primate and rodent literatures, identifying 5-Hz rhythmic co-firing of neurons as a signature of assembly dynamics underpinning limbic-cortical interactions during short-term memory. [ABSTRACT FROM AUTHOR]

Highlights: [•] Alternation procedures in rodents are highly sensitive to manipulations of the hippocampus. [•] However as they require hand testing, they are low throughput and stressful for the animal. [•] An automated maze was developed for assessing alternation performance in mice. [•] Alternation performance was shown to be impaired in mice with lesions to the hippocampus. [Copyright &y& Elsevier]