Psychedelics reopen the social reward learning critical period

Romain Nardou, Edward Sawyer, Young Jun Song, Makenzie Wilkinson, Yasmin Padovan-Hernandez, Júnia Lara de Deus, Noelle Wright, Carine Lama, Sehr Faltin, Loyal A. Goff, Genevieve L. Stein-O’Brien and Gül Dölen ()
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Romain Nardou: Johns Hopkins University, School of Medicine
Edward Sawyer: Johns Hopkins University, School of Medicine
Young Jun Song: Johns Hopkins University, School of Medicine
Makenzie Wilkinson: Johns Hopkins University, School of Medicine
Yasmin Padovan-Hernandez: Johns Hopkins University, School of Medicine
Júnia Lara de Deus: Johns Hopkins University, School of Medicine
Noelle Wright: Johns Hopkins University, School of Medicine
Carine Lama: Johns Hopkins University, School of Medicine
Sehr Faltin: Johns Hopkins University, School of Medicine
Loyal A. Goff: Johns Hopkins University, School of Medicine
Genevieve L. Stein-O’Brien: Johns Hopkins University, School of Medicine
Gül Dölen: Johns Hopkins University, School of Medicine

Nature, 2023, vol. 618, issue 7966, 790-798

Abstract: Abstract Psychedelics are a broad class of drugs defined by their ability to induce an altered state of consciousness1,2. These drugs have been used for millennia in both spiritual and medicinal contexts, and a number of recent clinical successes have spurred a renewed interest in developing psychedelic therapies3–9. Nevertheless, a unifying mechanism that can account for these shared phenomenological and therapeutic properties remains unknown. Here we demonstrate in mice that the ability to reopen the social reward learning critical period is a shared property across psychedelic drugs. Notably, the time course of critical period reopening is proportional to the duration of acute subjective effects reported in humans. Furthermore, the ability to reinstate social reward learning in adulthood is paralleled by metaplastic restoration of oxytocin-mediated long-term depression in the nucleus accumbens. Finally, identification of differentially expressed genes in the ‘open state’ versus the ‘closed state’ provides evidence that reorganization of the extracellular matrix is a common downstream mechanism underlying psychedelic drug-mediated critical period reopening. Together these results have important implications for the implementation of psychedelics in clinical practice, as well as the design of novel compounds for the treatment of neuropsychiatric disease.

Date: 2023
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DOI: 10.1038/s41586-023-06204-3

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