Depressive DisordersAnxiety DisordersNeuroimaging & Brain MeasuresMedicinal Chemistry & Drug Development

Serotonin and brain function: a tale of two receptors

This theory-building article (2017) argues that the serotonin (5-HT) 2a receptor (psychedelics) is responsible for active coping (plasticity) of adversity, whereas the 5-HT1a receptor (SSRIs) only leads to passive coping (stress reduction). The theory offers an explanation for the different pathways and outcomes of psychedelics and more traditional medications/ways of coping.

Authors

  • Robin Carhart-Harris
  • David Nutt

Published

Journal of Psychopharmacology
meta Study

Abstract

Previous attempts to identify a unified theory of brain serotonin function have largely failed to achieve consensus. In this present synthesis, we integrate previous perspectives with new and older data to create a novel bipartite model centred on the view that serotonin neurotransmission enhances two distinct adaptive responses to adversity, mediated in large part by its two most prevalent and researched brain receptors: the 5-HT1A and 5-HT2A receptors. We propose that passive coping (i.e. tolerating a source of stress) is mediated by postsynaptic 5-HT1AR signalling and characterised by stress moderation. Conversely, we argue that active coping (i.e. actively addressing a source of stress) is mediated by 5-HT2AR signalling and characterised by enhanced plasticity (defined as capacity for change). We propose that 5-HT1AR-mediated stress moderation may be the brain’s default response to adversity but that an improved ability to change one’s situation and/or relationship to it via 5-HT2AR-mediated plasticity may also be important - and increasingly so as the level of adversity reaches a critical point. We propose that the 5-HT1AR pathway is enhanced by conventional 5-HT reuptake blocking antidepressants such as the selective serotonin reuptake inhibitors (SSRIs), whereas the 5-HT2AR pathway is enhanced by 5-HT2AR-agonist psychedelics. This bipartite model purports to explain how different drugs (SSRIs and psychedelics) that modulate the serotonergic system in different ways, can achieve complementary adaptive and potentially therapeutic outcomes.

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Research Summary of 'Serotonin and brain function: a tale of two receptors'

Introduction

Earlier attempts to define a unifying function for brain serotonin (5-HT) have been inconclusive, in part because the serotonergic system is highly diverse: multiple receptor subtypes, broad innervation and paracrine-style signalling complicate simple accounts. The authors argue that progress is most likely by focusing on receptor-specific actions, and they select two receptors for detailed consideration: the inhibitory postsynaptic 5-HT1A receptor (5-HT1AR), densely expressed in limbic regions, and the excitatory 5-HT2A receptor (5-HT2AR), abundant in high-level cortex and especially associative/default-mode network regions. Prior literature links 5-HT broadly with stress moderation, patience and affect regulation, but the role of 5-HT2AR signalling in plasticity and the pronounced psychological effects of direct 5-HT2AR agonists (classic psychedelics) motivates a reappraisal. Rl and colleagues set out to synthesise animal, human pharmacological, neuroimaging and clinical data into a bipartite model in which 5-HT transmission supports two complementary adaptive responses to adversity. In this model, postsynaptic 5-HT1AR signalling mediates a ‘‘passive coping’’ response characterised by stress moderation and improved tolerance, whereas 5-HT2AR signalling mediates an ‘‘active coping’’ response associated with heightened plasticity and an increased capacity for change. The paper aims to integrate evidence for receptor localisation and function, behavioural correlates (impulsivity, aggression, anxiety, learning), clinical findings with SSRIs, MDMA and psychedelics, and conceptual models such as an extra-pharmacological (set–setting–trait–dose) framework and the entropic brain hypothesis.

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Critical Period Plasticity as a Framework for Psychedelic-Assisted Psychotherapy

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Psychedelics for Brain Injury: A Mini-Review

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Does psychedelic therapy have a transdiagnostic action and prophylactic potential?

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Decreased brain modularity after psilocybin therapy for depression

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Relational Processes in Ayahuasca Groups of Palestinians and Israelis

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Symptom specificity of ayahuasca's effect on depressive symptoms

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Clinical and biological predictors of psychedelic response in the treatment of psychiatric and addictive disorders: a systematic review

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A qualitative and quantitative account of patient’s experiences of ketamine and its antidepressant properties

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Positive expectations predict improved mental-health outcomes linked to psychedelic microdosing

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112 cited
The entropic tongue: Disorganization of natural language under LSD

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24 cited
Effect of lysergic acid diethylamide (LSD) on reinforcement learning in humans

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Pivotal Mental States

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Improved colour blindness symptoms associated with recreational psychedelic use: Results from the Global Drug Survey 2017

Ferris, J. A., Nutt, D. J. · Drug Science Policy and Law (2020)

7 cited
Therapeutic effects of classic serotonergic psychedelics: A systematic review of modern-era clinical studies

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Serotonergic psychedelics LSD & psilocybin increase the fractal dimension of cortical brain activity in spatial and temporal domains

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Psychedelic science in post-COVID-19 psychiatry

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Post-Psychedelic Reductions in Experiential Avoidance Are Associated With Decreases in Depression Severity and Suicidal Ideation

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82 cited
Me, myself, bye: regional alterations in glutamate and the experience of ego dissolution with psilocybin

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Depression, Mindfulness, and Psilocybin: Possible Complementary Effects of Mindfulness Meditation and Psilocybin in the Treatment of Depression. A Review

Heuschkel, K., Kuypers, K. P. C. · Frontiers in Psychiatry (2020)

63 cited
Dissolving the self: Active inference, psychedelics, and ego-dissolution

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Natural Psychoplastogens As Antidepressant Agents

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Microdosing psychedelics: Demographics, practices, and psychiatric comorbidities.

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55 cited
Learning to Let Go: A Cognitive-Behavioral Model of How Psychedelic Therapy Promotes Acceptance

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Therapeutic mechanisms of psilocybin: Changes in amygdala and prefrontal functional connectivity during emotional processing after psilocybin for treatment-resistant depression

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155 cited
Long-term follow-up of psilocybin-assisted psychotherapy for psychiatric and existential distress in patients with life-threatening cancer

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292 cited
Novel pharmacological targets in drug development for the treatment of anxiety and anxiety-related disorders

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REBUS and the Anarchic Brain: Toward a Unified Model of the Brain Action of Psychedelics

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Psychedelic drugs-a new era in psychiatry?

Nutt, D. J. · Dialogues in Clinical Neuroscience (2019)

Sensitization to the prosocial effects of 3,4-methylenedioxymethamphetamine (MDMA)

Curry, D. W., Berro, L. F., Belkoff, A. R. et al. · Neuropharmacology (2019)

Psychedelics as a treatment for disorders of consciousness

Scott, G., Carhart-Harris, R. L. · Neuroscience of Consciousness (2019)

States and traits related to the quality and consequences of psychedelic experiences

Russ, S. L., Carhart-Harris, R. L., Maruyama, G. et al. · Psychology of Consciousness Theory Research and Practice (2019)

Recreational use of psychedelics is associated with elevated personality trait openness: Exploration of associations with brain serotonin markers

Erritzoe, D., Smith, J. M., Fisher, P. M. et al. · Journal of Psychopharmacology (2019)

How do psychedelics work?

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Increased amygdala responses to emotional faces after psilocybin for treatment-resistant depression

Roseman, L., Demetriou, L., Wall, M. B. et al. · Neuropharmacology (2018)

Exploring the effect of microdosing psychedelics on creativity in an open-label natural setting

Prochazkova, L., Lippelt, D. P., Colzato, L. S. et al. · Psychopharmacology (2018)

More realistic forecasting of future life events after psilocybin for treatment-resistant depression

Lyons, T., Carhart-Harris, R. L. · Frontiers in Psychology (2018)

49 cited
Whole-brain multimodal neuroimaging model using serotonin receptor maps explains non-linear functional effects of LSD

Deco, G., Cruzat, J., Cabral, J. et al. · Current Biology (2018)

DMT models the near-death experience

Timmermann, C., Roseman, L., Williams, L. et al. · Frontiers in Psychology (2018)

N, N-Dimethyltryptamine (DMT), an Endogenous Hallucinogen: Past, Present, and Future Research to Determine Its Role and Function

Barker, S. · Frontiers in Neuroscience (2018)

Dark Classics in Chemical Neuroscience: N, N-Dimethyltryptamine (DMT)

Cameron, L. P. · ACS Chemical Neuroscience (2018)

Effects of psilocybin therapy on personality structure

Erritzoe, D., Roseman, L., Nour, M. R. et al. · Acta Psychiatrica Scandinavica (2018)

219 cited
Psilocybin and MDMA reduce costly punishment in the Ultimatum Game

Gabay, A. S., Carhart-Harris, R. L., Mazibuko, N. et al. · Scientific Reports (2018)

The entropic brain - revisited

Carhart-Harris, R. L. · Neuropharmacology (2018)

The Meaning-Enhancing Properties of Psychedelics and Their Mediator Role in Psychedelic Therapy, Spirituality, and Creativity

Hartogsohn, I. · Frontiers in Human Neuroscience (2018)

Unifying theories of psychedelic drug effects

Swanson, L. R. · Frontiers in Pharmacology (2018)

Psychedelics and the essential importance of context

Carhart-Harris, R. L., Roseman, L., Haijen, E. C. H. M. et al. · Journal of Psychopharmacology (2018)

Increased nature relatedness and decreased authoritarian political views after psilocybin for treatment-resistant depression

Lyons, T., Carhart-Harris, R. L. · Journal of Psychopharmacology (2018)

Quality of acute psychedelic experience predicts therapeutic efficacy of psilocybin for treatment-resistant depression

Roseman, L., Nutt, D. J., Carhart-Harris, R. L. · Frontiers in Pharmacology (2018)

Psilocybin with psychological support for treatment-resistant depression: six-month follow-up

Carhart-Harris, R. L., Bolstridge, &. M., Day, C. M. J. et al. · Psychopharmacology (2017)

Psilocybin with psychological support improves emotional face recognition in treatment-resistant depression

Stroud, J., Freeman, T. P., Leech, R. et al. · Psychopharmacology (2017)

88 cited
Psychedelics and connectedness

Carhart-Harris, R. L., Erritzoe, D., Haijen, E. C. H. M. et al. · Psychopharmacology (2017)

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Serotonin and brain function: a tale of two... — Research Summary & Context | Blossom