Blocking human fear memory with the matrix metalloproteinase inhibitor doxycycline
Open accessAbstract
Learning to predict threat is a fundamental ability of many biological organisms, and a laboratory model for anxiety disorders. Interfering with such memories in humans would be of high clinical relevance. On the basis of studies in cell cultures and slice preparations, it is hypothesised that synaptic remodelling required for threat learning involves the extracellular enzyme matrix metalloproteinase (MMP) 9. However, in vivo evidence for this proposal is lacking. Here we investigate human Pavlovian fear conditioning under the blood-brain barrier crossing MMP inhibitor doxycyline in a pre-registered, randomised, double-blind, placebo-controlled trial. We find that recall of threat memory, measured with fear-potentiated startle 7 days after acquisition, is attenuated by ~60% in individuals who were under doxycycline during acquisition. This threat memory impairment is also reflected in increased behavioural surprise signals to the conditioned stimulus during subsequent re-learning, and already late during initial acquisition. Our findings support an emerging view that extracellular signalling pathways are crucially required for threat memory formation. Furthermore, they suggest novel pharmacological methods for primary prevention and treatment of posttraumatic stress disorder.
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Similar impairments of fear recall and additional enhancements of fear extinction are observed following acute antibiotic exposure in humans and rodents.
“Similar impairments of fear recall and additional enhancements of fear extinction are observed following acute antibiotic exposure in humans and rodents (Bach et al., 2018;Davis et al., 2006;Rodrigues et al., 2014).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Bach et al., 2018
The Results report approximately 60% less threat-memory retention in the human doxycycline group than in the placebo group. They also explicitly report no difference between groups in extinction. This paper therefore supports the fear-recall impairment but not the claimed enhancement of extinction; its trial did not study rodents. (LLM, conf=0.90)
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- Authors
- Bach, D. R., Tzovara, A., & Vunder, J.
- Affiliations
- Wellcome Centre for Human Neuroimaging (GB)
- University of Zurich (CH)
- Corresponding author
- Bach, D R
- ORCID
- Venue
- Molecular Psychiatry
- Published
- 2017-04-04
- Volume
- 23
- Issue
- 7
- Pages
- 1584-1589
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- PMC
- PMC5507298
- OpenAlex
- W2604366285
- Cited by
- 64
- References
- 54
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 9 · 2023: 6 · 2022: 5 · 2021: 7 · 2020: 9 · 2019: 9 · 2018: 8 · 2017: 2
- FWCI
- 4.39
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Molecular Psychiatry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by)
- UCL Discovery (University College London) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Science Foundation
- Wellcome Trust (091593, 091593/Z/10/Z)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (149586, 320030_1449586/1, 320030)
- Universität Zürich (320030_1449586/1)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- doxycycline, MMP-9, fear memory, fear conditioning, fear-potentiated startle, memory reconsolidation, threat memory, blood-brain barrier, synaptic remodeling, post-traumatic stress disorder, anxiety disorders
- MeSH terms
- Adult, Conditioning, Classical, Double-Blind Method, Doxycycline, Fear, Female, Humans, Learning, Male, Memory, Mental Recall, Reflex, Startle, Young Adult, Matrix Metalloproteinase Inhibitors
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