Hippocampal network oscillations at the interplay between innate anxiety and learned fear
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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.
KeywordsUnlearned innate anxiety Learned fear Posttraumatic stress disorder Extinction Oscillations Gamma Theta Sharp-wave ripple Dorsal and ventral hippocampus; amygdala Medial prefrontal cortex
This research was funded by grants, from the German Research Foundation (CRC779 TPB5 and STO488/6) and by the federal state of Saxony-Anhalt and the “European Regional Development Fund” (ERDF 2007–2013), Vorhaben: Centre for Behavioural Brain Sciences (CBBS) to Oliver Stork. Gürsel Çalışkan is funded by CBBS ScienceCampus financed by the Leibniz Association (SAS-2015-LIN-LWC).
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Conflict of interest
The authors declare that they have no conflict of interest.
is measure of synchrony between two LFP patterns based on changes in both amplitude and phase.
is measure of synchrony between two LFP patterns based on their phase similarity as a product of time. This measure is independent of amplitude changes in time and rather focuses on waveform similarity.
is a measure that gives information about the strength of LFP signal at a certain frequency range. In extracellular physiology, to determine the frequency of main oscillation power, scientists convert the LFP signal into a range of frequencies (Power Spectrum) as a function of their power in the LFP signal.
is a measure to determine the functional communication between two regions in the brain by measuring the similarity of simultaneously recorded LFP oscillation patterns based on their fluctuations in phase and/or amplitude. The synchrony of underlying cellular firing can also be detected by measuring whether cells fire at a particular phase of oscillations recorded locally or in a remote brain region.
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