Ventral hippocampus inactivation enhances the extinction of active avoidance responses in the presence of safety signals but leaves discrete trial operant active avoidance performance intact

Hippocampus. 2020 Sep;30(9):913-925. doi: 10.1002/hipo.23202. Epub 2020 Mar 4.

Abstract

The acquisition of active avoidance (AA) behavior is typically aided by the presence of two signals-the warning signal, which predicts the future occurrence of an aversive event (e.g., shocks), and the safety signal, which is presented upon successful avoidance of oncoming shocks. While the warning signal could be conceived to act as a Pavlovian fear cue, and is likely mediated by brain areas that underlie Pavlovian fear cue conditioning, the neural substrates underlying safety signaling are less clear, largely due to the unavailability of AA tasks that are devoid of an explicit warning signal. The present study sought to investigate the role of the ventral hippocampus (VH) in safety signaled AA performance acquired without an explicit warning signal, using a novel discrete trial paradigm. Adult male Long Evans rats were divided into two groups and trained to acquire AA responses with, or without a safety signal. Analysis of the acquisition and stable state performance data revealed that the availability of a safety signal alone did not improve the acquisition or performance of AA responses. Furthermore, post-training, reversible VH inactivation did not impact stable state avoidance behavior. However, extinction of avoidance responses was facilitated in the group trained with a safety signal, and this effect was further potentiated by VH inactivation. Additional elevated plus maze (EPM), light-dark box, and locomotor tests demonstrated that VH inactivation reduced anxiety without affecting locomotor activity. Taken together, these results demonstrate the importance of VH in the extinction of persistent pathological avoidance behavior when safety is signaled.

Keywords: anxiety; conditioned inhibition; conditioned reinforcement; operant active avoidance; safety signal; warning signal.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Avoidance Learning / drug effects
  • Avoidance Learning / physiology*
  • Conditioning, Operant / drug effects
  • Conditioning, Operant / physiology*
  • Extinction, Psychological / drug effects
  • Extinction, Psychological / physiology*
  • Fear / drug effects
  • Fear / physiology
  • Fear / psychology
  • GABA Agonists / administration & dosage
  • Hippocampus / drug effects
  • Hippocampus / physiology*
  • Locomotion / drug effects
  • Locomotion / physiology*
  • Male
  • Microinjections / methods
  • Rats
  • Rats, Long-Evans
  • Reinforcement, Psychology

Substances

  • GABA Agonists