Abstract

The mammalian hippocampal dentate gyrus is a unique memory circuit in which a subset of neurons is continuously generated throughout the lifespan. Previous studies have shown that the dentate gyrus neuronal population can hold fear memory traces (i.e., engrams) and that adult-born neurons (ABNs) support this process. However, it is unclear whether ABNs themselves hold fear memory traces. Therefore, we analyzed ABN activity at a population level across a fear conditioning paradigm. We found that fear learning did not recruit a distinct ABN population. In sharp contrast, a completely different ABN population was recruited during fear memory retrieval. We further provide evidence that ABN population activity remaps over time during the consolidation period. These results suggest that ABNs support the establishment of a fear memory trace in a different manner to directly holding the memory. Moreover, this activity remapping process in ABNs may support the segregation of memories formed at different times. These results provide new insight into the role of adult neurogenesis in the mammalian memory system.

Highlights

  • New neurons are continuously generated in the adult hippocampal dentate gyrus [1]

  • Memory consolidation depends on the sparse activity of adult-born neurons (ABNs) during rapid eye movement (REM) sleep [16]

  • We show evidence that ABN activity remaps over time during fear memory consolidation

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Summary

Introduction

New neurons are continuously generated in the adult hippocampal dentate gyrus [1]. This adult neurogenesis produces granular neurons that are similar to developmentally born granular neurons [2,3,4]. During their maturation, young adult-born neurons (ABNs) show properties that are distinct from those of developmentally born neurons, including higher synaptic plasticity and excitability [3,5,6,7,8] and lower input selectively and inhibitory inputs [9,10,11,12] These properties allow ABNs to be preferentially activated by novel stimuli [8,13,14] and could allow transitions in active cohorts of ABNs over time to achieve temporal separation and integration of different memories [12,15]. The mechanisms by which ABNs contribute to memory processing across time are still largely unknown

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