4.8 Article

Distinct nonuniform cable properties optimize rapid and efficient activation of fast-spiking GABAergic interneurons

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.0910716107

Keywords

cable models; dendrites; hippocampus; basket cell

Funding

  1. Bundesministerium fur Bildung und Forschung [01 GQ 0420]
  2. Deutsche Forschungsgemeinschaft [SFB 780/A5, TR 3/B10]
  3. Leibniz program
  4. Volkswagenstiftung [I/78 563-564]
  5. Norwegian Research Council [178670/V40]

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Fast-spiking, parvalbumin-expressing basket cells (BCs) play a key role in feedforward and feedback inhibition in the hippocampus. However, the dendritic mechanisms underlying rapid interneuron recruitment have remained unclear. To quantitatively address this question, we developed detailed passive cable models of BCs in the dentate gyrus based on dual somatic or somatodendritic recordings and complete morphologic reconstructions. Both specific membrane capacitance and axial resistivity were comparable to those of pyramidal neurons, but the average somatodendritic specific membrane resistance (R-m) was substantially lower in BCs. Furthermore, R-m was markedly nonuniform, being lowest in soma and proximal dendrites, intermediate in distal dendrites, and highest in the axon. Thus, the somatodendritic gradient of R-m was the reverse of that in pyramidal neurons. Further computational analysis revealed that these unique cable properties accelerate the time course of synaptic potentials at the soma in response to fast inputs, while boosting the efficacy of slow distal inputs. These properties will facilitate both rapid phasic and efficient tonic activation of BCs in hippocampal microcircuits.

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