Cellular and circuit features distinguish mouse dentate gyrus semilunar granule cells and granule cells activated during contextual memory formation

The dentate gyrus is critical for spatial memory formation and shows task-related activation of cellular ensembles considered as memory engrams. Semilunar granule cells (SGCs), a sparse dentate projection neuron subtype, were reported to be enriched among behaviorally activated neurons. By examining SGCs and granule cells (GCs) labeled during contextual memory formation in TRAP2 mice, we empirically tested competing hypotheses for GC and SGC recruitment into memory ensembles. Consistent with more excitable neurons being recruited into memory ensembles, SGCs showed greater sustained firing than GCs. Additionally, labeled SGCs showed less adapting firing than unlabeled SGCs. The lack of glutamatergic connections between behaviorally labeled SGCs and GCs in our recordings is inconsistent with SGC-driven local circuit feedforward excitation underlying ensemble recruitment. Moreover, there was little evidence for individual SGCs or labeled neuronal ensembles supporting lateral inhibition of unlabeled neurons. Instead, labeled GCs and SGCs received more spontaneous excitatory synaptic inputs than their unlabeled counterparts. Labeled neuronal pairs received more temporally correlated spontaneous excitatory synaptic inputs than labeled-unlabeled neuronal pairs. These findings challenge the proposal that SGCs drive dentate GC ensemble refinement, while supporting a role for intrinsic excitability and correlated inputs in preferential SGC recruitment to contextual memory engrams.