Ventral Striatal Dopamine Increases following Hippocampal Sharp-Wave Ripples

Abstract

The reactivation of task-related hippocampal activity during sharp-wave ripples (SWRs), often expressed as sequential "replay," is thought to contribute to behavior through both online and offline processes. Theories of replay-based learning and decision-making posit the need for replay events to be followed by an evaluative signal. Dopamine (DA) is a prime candidate for providing such a signal, particularly in the ventral striatum, where it reflects reward- and other prediction-error signals. Hippocampal activity influences mesolimbic dopamine signaling and neural activity in the ventral striatum, but it is unknown whether SWRs are coupled to ventral striatal DA release. To address this, we simultaneously recorded dorsal CA1 local field potentials to detect SWRs and measured ventral striatal DA concentration using fiber photometry in freely moving mice. We found a significant increase in DA following SWRs. This coupling was more prominent during offline rest than during periods of immobility during behavior, and was stronger following longer and higher-power SWRs. These results reveal coupling between hippocampal SWRs and striatal dopamine, providing a potential candidate mechanism through which internally generated hippocampal activity could engage evaluative signals during offline memory processing.