Behavior-Dependent Activity and Synaptic Organization of Septo-hippocampal GABAergic Neurons Selectively Targeting the Hippocampal CA3 Area

Neuron. 2017 Dec 20;96(6):1342-1357.e5. doi: 10.1016/j.neuron.2017.10.033. Epub 2017 Nov 30.


Rhythmic medial septal (MS) GABAergic input coordinates cortical theta oscillations. However, the rules of innervation of cortical cells and regions by diverse septal neurons are unknown. We report a specialized population of septal GABAergic neurons, the Teevra cells, selectively innervating the hippocampal CA3 area bypassing CA1, CA2, and the dentate gyrus. Parvalbumin-immunopositive Teevra cells show the highest rhythmicity among MS neurons and fire with short burst duration (median, 38 ms) preferentially at the trough of both CA1 theta and slow irregular oscillations, coincident with highest hippocampal excitability. Teevra cells synaptically target GABAergic axo-axonic and some CCK interneurons in restricted septo-temporal CA3 segments. The rhythmicity of their firing decreases from septal to temporal termination of individual axons. We hypothesize that Teevra neurons coordinate oscillatory activity across the septo-temporal axis, phasing the firing of specific CA3 interneurons, thereby contributing to the selection of pyramidal cell assemblies at the theta trough via disinhibition. VIDEO ABSTRACT.

Keywords: CA3; inhibition; medial septum; rhythm; subcortical; theta oscillations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Biotin / analogs & derivatives
  • Biotin / metabolism
  • CA3 Region, Hippocampal / cytology*
  • Cell Movement / genetics
  • Cell Movement / physiology*
  • Correlation of Data
  • GABAergic Neurons / metabolism
  • GABAergic Neurons / physiology*
  • GABAergic Neurons / ultrastructure
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Male
  • Matrix Attachment Region Binding Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Microscopy, Electron
  • Nerve Net / physiology*
  • Parvalbumins / metabolism
  • Septum of Brain / cytology*
  • Synapses / drug effects
  • Synapses / physiology*
  • Theta Rhythm / drug effects
  • Theta Rhythm / physiology


  • Bacterial Proteins
  • Luminescent Proteins
  • Matrix Attachment Region Binding Proteins
  • Parvalbumins
  • Satb1 protein, mouse
  • neurobiotin
  • yellow fluorescent protein, Bacteria
  • Biotin