Activity-dependent differences in function between proximal and distal Schaffer collaterals

J Neurophysiol. 2015 Jun 1;113(10):3646-62. doi: 10.1152/jn.00446.2014. Epub 2015 Apr 8.

Abstract

Axon conduction fidelity is important for signal transmission and has been studied in various axons, including the Schaffer collateral axons of the hippocampus. Previously, we reported that high-frequency stimulation (HFS) depresses Schaffer collateral excitability when assessed by whole-cell recordings from CA3 pyramidal cells but induces biphasic excitability changes (increase followed by decrease) in extracellular recordings of CA1 fiber volleys. Here, we examined responses from proximal (whole-cell or field-potential recordings from CA3 pyramidal cell somata) and distal (field-potential recordings from CA1 stratum radiatum) portions of the Schaffer collaterals during HFS and burst stimulation in hippocampal slices. Whole-cell and dual-field-potential recordings using 10-100-Hz HFS revealed frequency-dependent changes like those previously described, with higher frequencies producing more drastic changes. Dual-field-potential recordings revealed substantial differences in the response to HFS between proximal and distal regions of the Schaffer collaterals, with proximal axons depressing more strongly and only distal axons showing an initial excitability increase. Because CA3 pyramidal neurons normally fire in short bursts rather than long high-frequency trains, we repeated the dual recordings using 100-1,000-ms interval burst stimulation. Burst stimulation produced changes similar to those during HFS, with shorter intervals causing more drastic changes and substantial differences observed between proximal and distal axons. We suggest that functional differences between proximal and distal Schaffer collaterals may allow selective filtering of nonphysiological activity while maximizing successful conduction of physiological activity throughout an extensive axonal arbor.

Keywords: Schaffer collateral; action potential; burst stimulation; high-frequency stimulation; hyperexcitability.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Bicuculline / analogs & derivatives
  • Bicuculline / pharmacology
  • Biophysical Phenomena / physiology*
  • Dizocilpine Maleate / pharmacology
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Female
  • GABA-A Receptor Antagonists / pharmacology
  • Hippocampus / cytology*
  • In Vitro Techniques
  • Nerve Fibers / drug effects
  • Nerve Fibers / physiology*
  • Nerve Net / drug effects
  • Nerve Net / physiology*
  • Neurons / drug effects
  • Neurons / physiology*
  • Patch-Clamp Techniques
  • Phosphinic Acids / pharmacology
  • Propanolamines / pharmacology
  • Quinoxalines / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Reaction Time / drug effects

Substances

  • Excitatory Amino Acid Antagonists
  • GABA-A Receptor Antagonists
  • Phosphinic Acids
  • Propanolamines
  • Quinoxalines
  • CGP 55845A
  • bicuculline methiodide
  • FG 9041
  • Dizocilpine Maleate
  • Bicuculline