Differential Glutamatergic Inputs to Semilunar Granule Cells and Granule Cells Underscore Dentate Gyrus Projection Neuron Diversity

Abstract

Semilunar Granule Cells (SGCs) are sparse dentate gyrus projection neurons whose role in the dentate circuit, including pathway-specific inputs, remains unknown. We report that SGCs receive more frequent spontaneous excitatory synaptic inputs than granule cells (GCs). Dual GC-SGC recordings identified that SGCs receive stronger medial entorhinal cortex and associational synaptic drive but lack short-term facilitation of lateral entorhinal cortex inputs observed in GCs. Consistently, the probability of firing in response to medial perforant path input was greater in SGCs than in GCs. Additionally, the dendritic spine density on proximal and middle dendrites was higher in SGCs than GCs. However, the strength of commissural and supramammillary nuclear inputs and dendritic input integration, examined in passive morphometric simulations, did not differ between cell types. Activity-dependent labeling identified an overrepresentation of SGCs among neuronal ensembles in both mice trained in a spatial memory task and task-naive controls. The divergence of modality-specific entorhinal inputs to SGCs and GCs identified here can enable parallel processing of information streams and expand the computational capacity of the dentate gyrus.