Dorsal and Ventral Hippocampal Sharp-Wave Ripples Activate Distinct Nucleus Accumbens Networks

Neuron. 2020 Feb 19;105(4):725-741.e8. doi: 10.1016/j.neuron.2019.11.022. Epub 2019 Dec 18.

Abstract

Memories of positive experiences link places, events, and reward outcomes. These memories recruit interactions between the hippocampus and nucleus accumbens (NAc). Both dorsal and ventral hippocampus (dH and vH) project to the NAc, but it remains unknown whether dH and vH act in concert or separately to engage NAc representations related to space and reward. We recorded simultaneously from the dH, vH, and NAc of rats during an appetitive spatial task and focused on hippocampal sharp-wave ripples (SWRs) to identify times of memory reactivation across brain regions. Here, we show that dH and vH awake SWRs occur asynchronously and activate distinct and opposing patterns of NAc spiking. Only NAc neurons activated during dH SWRs were tuned to task- and reward-related information. These temporally and anatomically separable hippocampal-NAc interactions point to distinct channels of mnemonic processing in the NAc, with the dH-NAc channel specialized for spatial task and reward information. VIDEO ABSTRACT.

Keywords: hippocampus; learning; memory; neuronal network; nucleus accumbens; reward; sharp-wave ripple; spatial.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Hippocampus / cytology
  • Hippocampus / physiology*
  • Male
  • Nerve Net / cytology
  • Nerve Net / physiology*
  • Neurons / physiology*
  • Nucleus Accumbens / cytology
  • Nucleus Accumbens / physiology*
  • Rats
  • Rats, Long-Evans
  • Sleep / physiology