Remembering the “when”: Hebbian memory models for the time of past events

Abstract Humans and animals can remember how long ago specific events happened. Little is known about the neural mechanisms that enable remembering the “when” of memories stored for long durations in the episodic memory system – in contrast to interval-timing on the order of seconds and minutes. Based on a systematic exploration of neural coding, association and retrieval schemes, we develop model classes that span the space of possible mechanisms for the reconstruction of the time of past events. In concrete examples we show how network architecture, Hebbian plasticity, synaptic pruning or systems consolidation allow the retrieval of the time of past events. In a simulation, we demonstrate how these mechanisms would enable food caching animals like corvids to remember what they cached, where, and how long ago. To dissociate different hypotheses, we propose three kinds of novel, non-verbal experiments, that can be run with humans and animals. Our simulations predict the experimental results for different classes of models. Our study shows that remembering the “when” can be implemented by many biologically plausible mechanisms and that carefully designed experiments are needed to pin down the actual neural implementation of the memory for the time of past events in different species. Author summary Was it yesterday, a week ago, or perhaps even longer since I last ate pizza? Questions like these are typically easy to answer, because humans have a good sense of how long ago specific events happened. Research involving animals, such as food-caching birds, has revealed that they, too, can remember the “when” of past events. So far, little is known about the neuronal mechanisms that enable remembering the “when”. In this study, we explore systematically concrete hypotheses of how neural circuits, synaptic plasticity and ongoing restructuring of neural circuits allow remembering the “when”. We propose experiments, that could be done with humans or animals, to discriminate different biologically plausible mechanisms for remembering the “when”.