Hippocampal network oscillations at the interplay between innate anxiety and learned fear

Psychopharmacology (Berl). 2019 Jan;236(1):321-338. doi: 10.1007/s00213-018-5109-z. Epub 2018 Nov 11.


The hippocampus plays a central role as a hub for episodic memory and as an integrator of multimodal sensory information in time and space. Thereby, it critically determines contextual setting and specificity of episodic memories. It is also a key site for the control of innate anxiety states and involved in psychiatric diseases with heightened anxiety and generalized fear memory such as post-traumatic stress disorder (PTSD). Expression of both innate "unlearned" anxiety and "learned" fear requires contextual processing and engagement of a brain-wide network including the hippocampus together with the amygdala and medial prefrontal cortex. Strikingly, the hippocampus is also the site of emergence of oscillatory rhythms that coordinate information processing and filtering in this network. Here, we review data on how the hippocampal network oscillations and their coordination with amygdalar and prefrontal oscillations are engaged in innate threat evaluation. We further explore how such innate oscillatory communication might have an impact on contextualization and specificity of "learned" fear. We illustrate the partial overlap of fear and anxiety networks that are built by the hippocampus in conjunction with amygdala and prefrontal cortex. We further propose that (mal)-adaptive interplay via (dis)-balanced oscillatory communication between the anxiety network and the fear network may determine the strength of fear memories and their resistance to extinction.

Keywords: Dorsal and ventral hippocampus; amygdala; Extinction; Gamma; Learned fear; Medial prefrontal cortex; Oscillations; Posttraumatic stress disorder; Sharp-wave ripple; Theta; Unlearned innate anxiety.

Publication types

  • Review

MeSH terms

  • Amygdala / physiopathology
  • Animals
  • Anxiety Disorders / physiopathology*
  • Brain Mapping
  • Extinction, Psychological / physiology
  • Fear / physiology*
  • Hippocampus / physiopathology*
  • Humans
  • Instinct*
  • Memory, Episodic*
  • Nerve Net / physiopathology*
  • Prefrontal Cortex / physiopathology
  • Rodentia
  • Stress Disorders, Post-Traumatic / physiopathology*