Developmental emergence of hippocampal fast-field "ripple" oscillations in the behaving rat pups

Neuroscience. 2005;134(4):1423-30. doi: 10.1016/j.neuroscience.2005.05.030.

Abstract

Sharp wave and associated fast oscillatory ripples (140-200 Hz) in the cornu ammonis 1 region are the most synchronous hippocampal patterns in the adult rat. Spike sequences associated with sharp waves are believed to play a critical role in transferring transient memories from the hippocampus to the neocortex and the emergence of superfast ripples is pathognostic in temporal lobe epilepsy. Sharp waves in cornu ammonis 1 stratum radiatum are induced by a strong depolarization by the cornu ammonis 3 Schaffer collaterals, due to the synchronous discharge of cornu ammonis 3 pyramidal cells. Although during the first postnatal week, sharp-wave events are associated with hippocampal unit bursts in the pyramidal layer, ripple oscillations are absent. We investigated the emergence of fast-field oscillations in rat pups ranging from postnatal day 12-20 by recording with wire tetrodes in freely behaving pups and with 16-site linear silicon probes in head fixed animals. Cornu ammonis 1 pyramidal cell layer was determined by the presence of multiple unit activity and a reversal of the field potential in the deeper electrode sites. On-line verification of the recording sites was determined via an evoked response to commissural stimulation, showing a clear reversal in the field potential. Sharp wave-associated fast-field oscillations did not begin to emerge until the end of the second postnatal week and showed a gradual increase until day 18. Once ripples emerged, the intra-ripple frequency assumed adult values. The developmental time course of the ripple parallels the switch in the GABA(A) receptor-mediated signaling from excitation to inhibition. The time course may also reflect hitherto unidentified emergence of neuronal gap junctions.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Age Factors
  • Animals
  • Animals, Newborn
  • Behavior, Animal / physiology*
  • Biological Clocks
  • Electric Stimulation
  • Electroencephalography
  • Hippocampus / growth & development*
  • Hippocampus / physiology*
  • Male
  • Rats
  • Rats, Sprague-Dawley