Directional Theta Coherence in Prefrontal Cortical to Amygdalo-Hippocampal Pathways Signals Fear Extinction
Open accessAbstract
Theta oscillations are considered crucial mechanisms in neuronal communication across brain areas, required for consolidation and retrieval of fear memories. One form of inhibitory learning allowing adaptive control of fear memory is extinction, a deficit of which leads to maladaptive fear expression potentially leading to anxiety disorders. Behavioral responses after extinction training are thought to reflect a balance of recall from extinction memory and initial fear memory traces. Therefore, we hypothesized that the initial fear memory circuits impact behavioral fear after extinction, and more specifically, that the dynamics of theta synchrony in these pathways signal the individual fear response. Simultaneous multi-channel local field and unit recordings were obtained from the infralimbic prefrontal cortex, the hippocampal CA1 and the lateral amygdala in mice. Data revealed that the pattern of theta coherence and directionality within and across regions correlated with individual behavioral responses. Upon conditioned freezing, units were phase-locked to synchronized theta oscillations in these pathways, characterizing states of fear memory retrieval. When the conditioned stimulus evoked no fear during extinction recall, theta interactions were directional with prefrontal cortical spike firing leading hippocampal and amygdalar theta oscillations. These results indicate that the directional dynamics of theta-entrained activity across these areas guide changes in appraisal of threatening stimuli during fear memory and extinction retrieval. Given that exposure therapy involves procedures and pathways similar to those during extinction of conditioned fear, one therapeutical extension might be useful that imposes artificial theta activity to prefrontal cortical-amygdalo-hippocampal pathways that mimics the directionality signaling successful extinction recall.
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Following extinction of fear conditioning, spontaneous freezing to the extinguished conditioned stimulus is associated with synchronized theta rhythms among infralimbic cortex, CA1 and lateral amygdala.
“Following extinction of fear conditioning, spontaneous freezing to the extinguished CS, representing an inappropriate assessment of threat, is associated with synchronized theta rhythms among infralimbic cortex, CA1 and lateral amygdala134.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [134]
Following successful extinction of fear learning, infralimbic cortex spike firing leads the theta rhythm in hippocampus and lateral amygdala during presentations of the conditioned stimulus.
“Following successful extinction of fear learning, infralimbic cortex spike firing has been observed to lead the theta rhythm in hippocampus and lateral amygdala during presentations of the CS134.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [134]
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- Authors
- Lesting, J., Daldrup, T., Narayanan, V., Himpe, C., Seidenbecher, T., & Pape, H.-C.
- Affiliations
- University of Münster (DE)
- Corresponding author
- Pape, Hans-Christian
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-10-24
- Volume
- 8
- Issue
- 10
- Pages
- e77707
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3812006
- OpenAlex
- W1990940223
- Cited by
- 105
- References
- 61
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 6 · 2023: 10 · 2022: 5 · 2021: 11 · 2020: 8 · 2019: 10 · 2018: 8 · 2017: 7 · 2016: 11 · 2015: 12 · 2014: 3
- FWCI
- 4.75
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Deutsche Forschungsgemeinschaft (TP-A02, TRR‐58, SFB TRR 58)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- fear extinction, theta oscillations, prefrontal cortex, infralimbic cortex, hippocampal CA1, lateral amygdala, fear memory retrieval, phase locking, conditioned freezing, exposure therapy, anxiety disorders
- MeSH terms
- Amygdala, Animals, Conditioning, Psychological, Extinction, Psychological, Fear, Hippocampus, Learning, Male, Memory, Mice, Inbred C57BL, Neural Pathways, Mental Recall, Theta Rhythm, Prefrontal Cortex, Mice
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