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Cannabinoid modulation of functional connectivity within regions processing attentional salience.

Abstract

There is now considerable evidence to support the hypothesis that psychotic symptoms are the result of abnormal salience attribution, and that the attribution of salience is largely mediated through the prefrontal cortex, the striatum, and the hippocampus. Although these areas show differential activation under the influence of delta-9-tetrahydrocannabinol (delta-9-THC) and cannabidiol (CBD), the two major derivatives of cannabis sativa, little is known about the effects of these cannabinoids on the functional connectivity between these regions. We investigated this in healthy occasional cannabis users by employing event-related functional magnetic resonance imaging (fMRI) following oral administration of delta-9-THC, CBD, or a placebo capsule. Employing a seed cluster-based functional connectivity analysis that involved using the average time series from each seed cluster for a whole-brain correlational analysis, we investigated the effect of drug condition on functional connectivity between the seed clusters and the rest of the brain during an oddball salience processing task. Relative to the placebo condition, delta-9-THC and CBD had opposite effects on the functional connectivity between the dorsal striatum, the prefrontal cortex, and the hippocampus. Delta-9-THC reduced fronto-striatal connectivity, which was related to its effect on task performance, whereas this connection was enhanced by CBD. Conversely, mediotemporal-prefrontal connectivity was enhanced by delta-9-THC and reduced by CBD. Our results suggest that the functional integration of brain regions involved in salience processing is differentially modulated by single doses of delta-9-THC and CBD and that this relates to the processing of salient stimuli.

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  • Authors+Show Affiliations

    ,

    Department of Psychosis Studies, King's College London, Institute of Psychiatry, London, UK.

    ,

    1] Department of Psychosis Studies, King's College London, Institute of Psychiatry, London, UK [2] Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany.

    ,

    1] Instituto de Investigaciones Biomedicas August Pi i Sunyer (IDIBAPS), and Centro de Investigación Biomedica en Red en Salud Mental (CIBERSAM), Barcelona, Spain [2] Department of Psychiatry and Psychology, Hospital Clinic, University of Barcelona, Barcelona, Spain [3] INCT Translational Medicine (CNPq), Rio de Janeiro, Brazil.

    ,

    Department of Psychosis Studies, King's College London, Institute of Psychiatry, London, UK.

    ,

    1] INCT Translational Medicine (CNPq), Rio de Janeiro, Brazil [2] Department of Neuroscience and Behavior, Ribeirão Preto Medical School, University of São Paulo, São Paulo, Brazil.

    ,

    Department of Neuroimaging, King's College London, Institute of Psychiatry, London, UK.

    ,

    Department of Neuroimaging, King's College London, Institute of Psychiatry, London, UK.

    Department of Psychosis Studies, King's College London, Institute of Psychiatry, London, UK.

    Source

    MeSH

    Adult
    Attention
    Brain
    Brain Mapping
    Cannabidiol
    Cannabis
    Dronabinol
    Humans
    Magnetic Resonance Imaging
    Male
    Marijuana Smoking
    Neural Pathways
    Neuropsychological Tests
    Psychotropic Drugs

    Pub Type(s)

    Comparative Study
    Journal Article
    Research Support, Non-U.S. Gov't

    Language

    eng

    PubMed ID

    25249057

    Citation

    Bhattacharyya, Sagnik, et al. "Cannabinoid Modulation of Functional Connectivity Within Regions Processing Attentional Salience." Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, vol. 40, no. 6, 2015, pp. 1343-52.
    Bhattacharyya S, Falkenberg I, Martin-Santos R, et al. Cannabinoid modulation of functional connectivity within regions processing attentional salience. Neuropsychopharmacology. 2015;40(6):1343-52.
    Bhattacharyya, S., Falkenberg, I., Martin-Santos, R., Atakan, Z., Crippa, J. A., Giampietro, V., ... McGuire, P. (2015). Cannabinoid modulation of functional connectivity within regions processing attentional salience. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 40(6), pp. 1343-52. doi:10.1038/npp.2014.258.
    Bhattacharyya S, et al. Cannabinoid Modulation of Functional Connectivity Within Regions Processing Attentional Salience. Neuropsychopharmacology. 2015;40(6):1343-52. PubMed PMID: 25249057.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Cannabinoid modulation of functional connectivity within regions processing attentional salience. AU - Bhattacharyya,Sagnik, AU - Falkenberg,Irina, AU - Martin-Santos,Rocio, AU - Atakan,Zerrin, AU - Crippa,Jose A, AU - Giampietro,Vincent, AU - Brammer,Mick, AU - McGuire,Philip, Y1 - 2014/09/23/ PY - 2014/03/08/received PY - 2014/05/18/revised PY - 2014/06/12/accepted PY - 2014/9/25/entrez PY - 2014/9/25/pubmed PY - 2016/3/30/medline SP - 1343 EP - 52 JF - Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology JO - Neuropsychopharmacology VL - 40 IS - 6 N2 - There is now considerable evidence to support the hypothesis that psychotic symptoms are the result of abnormal salience attribution, and that the attribution of salience is largely mediated through the prefrontal cortex, the striatum, and the hippocampus. Although these areas show differential activation under the influence of delta-9-tetrahydrocannabinol (delta-9-THC) and cannabidiol (CBD), the two major derivatives of cannabis sativa, little is known about the effects of these cannabinoids on the functional connectivity between these regions. We investigated this in healthy occasional cannabis users by employing event-related functional magnetic resonance imaging (fMRI) following oral administration of delta-9-THC, CBD, or a placebo capsule. Employing a seed cluster-based functional connectivity analysis that involved using the average time series from each seed cluster for a whole-brain correlational analysis, we investigated the effect of drug condition on functional connectivity between the seed clusters and the rest of the brain during an oddball salience processing task. Relative to the placebo condition, delta-9-THC and CBD had opposite effects on the functional connectivity between the dorsal striatum, the prefrontal cortex, and the hippocampus. Delta-9-THC reduced fronto-striatal connectivity, which was related to its effect on task performance, whereas this connection was enhanced by CBD. Conversely, mediotemporal-prefrontal connectivity was enhanced by delta-9-THC and reduced by CBD. Our results suggest that the functional integration of brain regions involved in salience processing is differentially modulated by single doses of delta-9-THC and CBD and that this relates to the processing of salient stimuli. SN - 1740-634X UR - https://www.unboundmedicine.com/medline/citation/25249057/Cannabinoid_modulation_of_functional_connectivity_within_regions_processing_attentional_salience_ L2 - http://dx.doi.org/10.1038/npp.2014.258 DB - PRIME DP - Unbound Medicine ER -