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Repeated lysergic acid diethylamide (LSD) reverses stress-induced anxiety-like behavior, cortical synaptogenesis deficits and serotonergic neurotransmission decline

Abstract

Lysergic acid diethylamide (LSD) is a serotonergic psychedelic compound receiving increasing interest due to putative anxiolytic and antidepressant properties. However, the potential neurobiological mechanisms mediating these effects remain elusive. Employing in vivo electrophysiology, microionthophoresis, behavioral paradigms and morphology assays, we assessed the impact of acute and chronic LSD administration on anxiety-like behavior, on the cortical dendritic spines and on the activity of serotonin (5-HT) neurons originating in the dorsal raphe nucleus (DRN) in male mice exposed to chronic restraint stress. We found that while the acute intraperitoneal (i.p.) administration of LSD (5, 15 and 30 and 60 μg/kg) did not produce any anxiolytic or antidepressant effects in non-stressed mice, the dose of 30 µg/kg (daily for 7 days) prevented the stress-induced anxiety-like behavior and the stress-induced decrease of cortical spine densitiy. Interestingly, while LSD acutely decreased the firing activity of 5-HT neurons, repeated LSD increased their basal firing rate and restored the low 5-HT firing induced by stress. This effect was accompanied by a decreased inhibitory response of 5-HT neurons to microiontophoretic applications of the 5-HT1A agonist 8-OH-DPAT (8-hydroxy-N,N-dipropyl-2-aminotetralin). In conclusion, repeated LSD prevents the exacerbation of anxiety-like behavior following chronic stress exposure, but has no behavioral effects in non-stressed mice. These effects are paralleled by increased cortical spinogenesis and an enhancement of 5-HT neurotransmission which might be due to 5-HT1A receptors desensitization. Increased cortical spine density and enhancement of serotonergic neurotransmission may thus represent a candidate mechanism which mediate the therapeutic effects of serotonergic psychedelics on stress-induced anxiety.

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Fig. 1: Acute LSD treatment (5–60 μg/kg,i.p.) does not exert anxiolytic or antidepressant effects.
Fig. 2: Effects of repeated LSD treatment (5-30 μg/kg, i.p., once a day for 7 days) on open field test (OFT) performance in mice following chronic restraint stress (CS).
Fig. 3: Effects repeated LSD treatment (30 μg/kg,i.p., once a day for 7 days) on anxiety-like behavior, depressive like behavior and on mPFC spine density in mice following chronic restraint stress (CS).
Fig. 4: Effects of acute (10–30 μg/kg, i.p) and repeated LSD treatment (30 μg/kg, i.p., once a day for 7 days) on DRN 5-HT neurons.
Fig. 5: Effects of repeated LSD treatment (30 μg/kg, i.p, once a day, for 7 days) on DRN 5-HT neurons in mice following chronic restraint stress (CS).

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Funding

This work was supported by Grant 436986 from the CIHR, and the Quebec Network for Suicide, Mood Disorders, and Related Disorders (RQSHA, FRQS Grant 268065).

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DDG and GG designed research; DDG, AI, AM, JPE, MP, YER, ML-C, performed experiments and analyzed data; SC analyzed data and wrote manuscript; DDG, AI and GG wrote manuscript. GG supervised the whole work.

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Correspondence to Gabriella Gobbi.

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Competing interests

DDG is a consultant at Diamond Therapeutics Inc, Toronto, ON, Canada. GG and DDG are inventors of a pending patent regarding the use of LSD. DDG was a recipient of Fond Recherche Québec-Santé (FRQS) and a Canadian Institutes for Health Research (CIHR) postdoctoral fellowships. AI is a recipient of a CIHR, FRQS and a Quebec Autism Research Training Program (QART) postdoctoral fellowships. ML-C was a recipient of a Faculty of Medicine of McGill University/Ferring postdoctoral fellowship. The other authors declare no competing interests.

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De Gregorio, D., Inserra, A., Enns, J.P. et al. Repeated lysergic acid diethylamide (LSD) reverses stress-induced anxiety-like behavior, cortical synaptogenesis deficits and serotonergic neurotransmission decline. Neuropsychopharmacol. 47, 1188–1198 (2022). https://doi.org/10.1038/s41386-022-01301-9

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