Cell-Type-Specific Changes in Intrinsic Excitability in the Subiculum following Learning and Exposure to Novel Environmental Contexts

eNeuro. 2019 Jan 4;5(6):ENEURO.0484-18.2018. doi: 10.1523/ENEURO.0484-18.2018. eCollection 2018 Nov-Dec.

Abstract

The subiculum is the main target of the hippocampal region CA1 and is the principle output region of the hippocampus. The subiculum is critical to learning and memory, although it has been relatively understudied. There are two functional types of principle neurons within the subiculum: regular spiking (RS) and burst spiking (BS) neurons. To determine whether these cell types are differentially modified by learning-related experience, we performed whole-cell patch clamp recordings from male mouse brain slices following contextual fear conditioning (FC) and memory retrieval relative to a number of control behavioral paradigms. RS cells, but not BS cells, displayed a greater degree of experience-related plasticity in intrinsic excitability measures [afterhyperpolarization (AHP), input resistance (Rinput), current required to elicit a spike], with fear conditioned animals having generally more excitable RS cells compared to naïve controls. Furthermore, we found that the relative proportion of RS to BS neurons is modified by the type of exposure, with the lowest proportion of BS subicular cells occurring in animals that underwent contextual FC followed by a retrieval test. These studies indicate that pyramidal neurons in the subiculum undergo experience- and learning-related plasticity in intrinsic properties in a cell-type-specific manner. As BS and RS cells are thought to convey distinct types of information, this plasticity may be particularly important in encoding, consolidating, and recalling spatial information by modulating information flow from the hippocampus to cortical regions.

Keywords: burst spiking; contextual fear conditioning; intrinsic excitability; plasticity; regular spiking; subiculum.

Publication types

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

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Conditioning, Classical / drug effects
  • Conditioning, Classical / physiology*
  • Electric Stimulation
  • Electroshock
  • Environment*
  • Excitatory Amino Acid Antagonists / pharmacology
  • Fear / physiology*
  • GABA Antagonists / pharmacology
  • Hippocampus / cytology*
  • Hippocampus / physiology
  • In Vitro Techniques
  • Kynurenic Acid / pharmacology
  • Male
  • Memory / drug effects
  • Memory / physiology
  • Mice
  • Mice, Inbred C57BL
  • Neurons / classification
  • Neurons / drug effects
  • Neurons / physiology*
  • Pyridazines / pharmacology

Substances

  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • Pyridazines
  • gabazine
  • Kynurenic Acid