Adult born dentate granule cells evoke CA3 activity with a gain that increases along maturation

Abstract

Hippocampal granule cells (GCs) are among the few neurons that are born throughout mammalian lifespan. It has been shown that young adult born GCs (4 weeks old) are transiently hyperplastic and excitable compared to mature ones (8 weeks old). While their inputs are well characterized, only a few studies address the maturation of GCs outputs. Here we aim to investigate the influence of developing adult born GCs on CA3, its main target. We hypothesize that evoked activity in CA3 reflects transient properties of young GCs. To explore this possibility, we performed optical stimulation of a cohort of adult born GCs expressing channelrhodopsin-2 in awake behaving mice while recording neuronal activity in CA3. We used different frequencies of stimulation at variable laser intensities to stimulate young and mature GCs. We found that mature GCs recruit more CA3 single unit activity, with frequency dependent facilitation. Evoked local field potentials followed a similar pattern. Interestingly, a small subset of putative pyramidal CA3 cells presented significantly high spiking levels as long as 50 ms after the light pulse. Only mature GCs were able to evoke this sustained activity. Is this persistent excitability caused by attractor dynamics? Do adult born neurons reshape de architecture of recurrent CA3 networks? These results open new challenges regarding the function of adult hippocampal neurogenesis and mnemonic networks dynamics dependent on the neurogenic niche.