Pyramidal Cell-Interneuron Circuit Architecture and Dynamics in Hippocampal Networks

Neuron. 2017 Oct 11;96(2):505-520.e7. doi: 10.1016/j.neuron.2017.09.033.


Excitatory control of inhibitory neurons is poorly understood due to the difficulty of studying synaptic connectivity in vivo. We inferred such connectivity through analysis of spike timing and validated this inference using juxtacellular and optogenetic control of presynaptic spikes in behaving mice. We observed that neighboring CA1 neurons had stronger connections and that superficial pyramidal cells projected more to deep interneurons. Connection probability and strength were skewed, with a minority of highly connected hubs. Divergent presynaptic connections led to synchrony between interneurons. Synchrony of convergent presynaptic inputs boosted postsynaptic drive. Presynaptic firing frequency was read out by postsynaptic neurons through short-term depression and facilitation, with individual pyramidal cells and interneurons displaying a diversity of spike transmission filters. Additionally, spike transmission was strongly modulated by prior spike timing of the postsynaptic cell. These results bridge anatomical structure with physiological function.

Keywords: cell assemblies; circuits; cooperativity; hippocampus; interneuron; lognormal; pyramidal cell; short-term plasticity; spike transmission; synchrony.

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • CA1 Region, Hippocampal / chemistry
  • CA1 Region, Hippocampal / cytology
  • CA1 Region, Hippocampal / physiology*
  • Female
  • Interneurons / chemistry
  • Interneurons / physiology*
  • Male
  • Mice
  • Mice, Transgenic
  • Nerve Net / chemistry
  • Nerve Net / cytology
  • Nerve Net / physiology*
  • Optogenetics / methods
  • Pyramidal Cells / chemistry
  • Pyramidal Cells / physiology*
  • Random Allocation