Selective Routing of Spatial Information Flow from Input to Output in Hippocampal Granule Cells

Dentate gyrus granule cells (GCs) connect the entorhinal cortex to the hippocampal CA3 region, but how they process spatial information remains enigmatic. To examine the role of GCs in spatial coding, we measured excitatory postsynaptic potentials (EPSPs) and action potentials (APs) in head-fixed mice running on a linear belt. Intracellular recording from morphologically identified GCs revealed that most cells were active, but activity level varied over a wide range. Whereas only ∼5% of GCs showed spatially tuned spiking, ∼50% received spatially tuned input. Thus, the GC population broadly encodes spatial information, but only a subset relays this information to the CA3 network. Fourier analysis indicated that GCs received conjunctive place-grid-like synaptic input, suggesting code conversion in single neurons. GC firing was correlated with dendritic complexity and intrinsic excitability, but not extrinsic excitatory input or dendritic cable properties. Thus, functional maturation may control input-output transformation and spatial code conversion. [Display omitted] •>50% of hippocampal GCs are active, but activity level varies over a wide range•∼5% of GCs are place cells, but ∼50% receive spatially tuned synaptic input•Mixed input of GCs constrains models of grid-place code conversion•GC firing is controlled by intrinsic excitability Zhang et al. simultaneously measure subthreshold EPSP and suprathreshold AP activity in morphologically identified dentate gyrus GCs in mice during spatial navigation, using intracellular patch-clamp recording. Although only a minor fraction of GCs shows spatially tuned spiking, a major fraction receives spatially tuned synaptic input. Intrinsic excitability controls input-output conversion.