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

Neuron. 2020 Sep 23;107(6):1212-1225.e7. doi: 10.1016/j.neuron.2020.07.006. Epub 2020 Aug 6.

Abstract

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.

Keywords: EPSPs; action potential threshold; code conversion; dentate gyrus granule cells; grid cells; intracellular in vivo recording; intrinsic excitability; place cells; sparse coding; spatial navigation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials
  • Animals
  • CA3 Region, Hippocampal / cytology
  • CA3 Region, Hippocampal / physiology*
  • Cells, Cultured
  • Dentate Gyrus / cytology
  • Dentate Gyrus / physiology*
  • Excitatory Postsynaptic Potentials*
  • Female
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neurons / physiology*
  • Spatial Navigation*