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Psilocybin analog 4-OH-DiPT enhances fear extinction and GABAergic inhibition of principal neurons in the basolateral amygdala

Neuropsychopharmacology volume 49, pages 854–863 (2024)Cite this article

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Abstract

Psychedelics such as psilocybin show great promise for the treatment of depression and PTSD, but their long duration of action poses practical limitations for patient access. 4-OH-DiPT is a fast-acting and shorter-lasting derivative of psilocybin. Here we characterized the pharmacological profile of 4-OH-DiPT and examined its impact on fear extinction learning as well as a potential mechanism of action. First, we profiled 4-OH-DiPT at all 12 human 5-HT GPCRs. 4-OH-DiPT showed strongest agonist activity at all three 5-HT2A/2B/2C receptors with near full agonist activity at 5-HT2A. Notably, 4-OH-DiPT had comparable activity at mouse and human 5-HT2A/2B/2C receptors. In a fear extinction paradigm, 4-OH-DiPT significantly reduced freezing responses to conditioned cues in a dose-dependent manner with a greater potency in female mice than male mice. Female mice that received 4-OH-DiPT before extinction training had reduced avoidance behaviors several days later in the light dark box, elevated plus maze and novelty-suppressed feeding test compared to controls, while male mice did not show significant differences. 4-OH-DiPT produced robust increases in spontaneous inhibitory postsynaptic currents (sIPSCs) in basolateral amygdala (BLA) principal neurons and action potential firing in BLA interneurons in a 5-HT2A-dependent manner. RNAscope demonstrates that Htr2a mRNA is expressed predominantly in BLA GABA interneurons, Htr2c mRNA is expressed in both GABA interneurons and principal neurons, while Htr2b mRNA is absent in the BLA. Our findings suggest that 4-OH-DiPT activates BLA interneurons via the 5-HT2A receptor to enhance GABAergic inhibition of BLA principal neurons, which provides a potential mechanism for suppressing learned fear.

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Fig. 1: Pharmacological profile of 4-OH-DiPT at the 5-HTome.
Fig. 2: 4-OH-DiPT-paired extinction training reduces conditioned fear expression and decreases avoidance behavior in female mice.
Fig. 3: 4-OH-DiPT enhances spontaneous inhibitory tone on BLA principal neurons.
Fig. 4: 4-OH-DiPT induces AP firing in BLA interneurons via 5-HT2A activation.
Fig. 5: Expression of Htr2a is localized to interneurons in the basolateral amygdala.

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Funding

Funding

This work was supported by National Institutes of Health Grants R01MH121454, DA047269 and R01DA035217 (to QSL), R35GM133421 (to JDM), and F31DA054759 (to VF). TJK is a member of the Medical Scientist Training Program at MCW, which is partially supported by a training grant from NIGMS T32-GM080202. It was also partially funded through the Research and Education Initiative Fund, a component of the Advancing a Healthier Wisconsin endowment at MCW.

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Authors and Affiliations

  1. Department of Pharmacology and Toxicology, Medical College of Wisconsin, Milwaukee, WI, 53226, USA

    Thomas J. Kelly, Lianwei Mu, Xiaojie Liu, Ying Hu, Vladislav Friedman, Hao Yu, Wantang Su & Qing-song Liu

  2. Department of Cell Biology, Neurobiology and Anatomy, Medical College of Wisconsin, Milwaukee, WI, 53226, USA

    Emma M. Bonniwell & John D. McCorvy

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  1. Thomas J. Kelly
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Contributions

TJK, QSL, and JDM designed the experiments. TJK, EB, LM, HY, XJ, YH, WS, and VF performed the experiments. TJK wrote the initial draft. TJK, QSL, JDM, and EB wrote the revised manuscript. VF edited the manuscript. JDM supervised the 5-HT receptor BRET experiments and were conducted by EMB.

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Correspondence to John D. McCorvy or Qing-song Liu.

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Kelly, T.J., Bonniwell, E.M., Mu, L. et al. Psilocybin analog 4-OH-DiPT enhances fear extinction and GABAergic inhibition of principal neurons in the basolateral amygdala. Neuropsychopharmacol. 49, 854–863 (2024). https://doi.org/10.1038/s41386-023-01744-8

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