Neurometabolic profile of the amygdala in smokers assessed with 1H-magnetic resonance spectroscopy
Tobacco smoking is one of the main causes of premature death worldwide and quitting success remains low, highlighting the need to understand the neurobiological mechanisms underlying relapse. Preclinical models have shown that the amygdala and glutamate play an important role in nicotine addiction....
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| Format: | Article |
| Language: | English |
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Elsevier
2024-03-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S105381192400020X |
| _version_ | 1797301625545555968 |
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| author | Colette A Steinegger Niklaus Zoelch Andreas Hock Anke Henning Etna JE Engeli Christopher R Pryce Erich Seifritz Marcus Herdener Lea M Hulka |
| author_facet | Colette A Steinegger Niklaus Zoelch Andreas Hock Anke Henning Etna JE Engeli Christopher R Pryce Erich Seifritz Marcus Herdener Lea M Hulka |
| author_sort | Colette A Steinegger |
| collection | DOAJ |
| description | Tobacco smoking is one of the main causes of premature death worldwide and quitting success remains low, highlighting the need to understand the neurobiological mechanisms underlying relapse. Preclinical models have shown that the amygdala and glutamate play an important role in nicotine addiction. The aims of this study were to compare glutamate and other metabolites in the amygdala between smokers and controls, and between different smoking states. Furthermore, associations between amygdalar metabolite levels and smoking characteristics were explored.A novel non-water-suppressed proton magnetic resonance spectroscopy protocol was applied to quantify neurometabolites in 28 male smokers (≥15 cigarettes/day) and 21 non-smoking controls, matched in age, education, verbal IQ, and weekly alcohol consumption. Controls were measured once (baseline) and smokers were measured in a baseline state (1–3 h abstinence), during withdrawal (24 h abstinence) and in a satiation state (directly after smoking). Baseline spectroscopy data were compared between groups by independent t-tests or Mann-Whitney-U tests. Smoking state differences were investigated by repeated-measures analyses of variance (ANOVAs). Associations between spectroscopy data and smoking characteristics were explored using Spearman correlations.Good spectral quality, high anatomical specificity (98% mean gray matter) and reliable quantification of most metabolites of interest were achieved in the amygdala. Metabolite levels did not differ between groups, but smokers showed significantly higher glutamine levels at baseline than satiation. Glx levels were negatively associated with pack-years and smoking duration.In summary, this study provides first insights into the neurometabolic profile of the amygdala in smokers with high anatomical specificity. By applying proton magnetic resonance spectroscopy, neurometabolites in smokers during different smoking states and non-smoking controls were quantified reliably. A significant shift in glutamine levels between smoking states was detected, with lower concentrations in satiation than baseline. The negative association between Glx levels and smoking quantity and duration may imply altered glutamate homeostasis with more severe nicotine addiction. |
| first_indexed | 2024-03-07T23:25:17Z |
| format | Article |
| id | doaj.art-ee1077f5354741638b67219350c494b5 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-03-07T23:25:17Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-ee1077f5354741638b67219350c494b52024-02-21T05:24:43ZengElsevierNeuroImage1095-95722024-03-01288120525Neurometabolic profile of the amygdala in smokers assessed with 1H-magnetic resonance spectroscopyColette A Steinegger0Niklaus Zoelch1Andreas Hock2Anke Henning3Etna JE Engeli4Christopher R Pryce5Erich Seifritz6Marcus Herdener7Lea M Hulka8Center for Addictive Disorders, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Selnaustrasse 9, Zurich 8001, Switzerland; Corresponding author.Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Switzerland; Institute of Forensic Medicine, Department of Forensic Medicine and Imaging, University of Zurich, Zurich, Switzerland; Institute for Biomedical Engineering, University and Swiss Federal Institute of Technology Zurich, Zurich, SwitzerlandDepartment of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Switzerland; Institute for Biomedical Engineering, University and Swiss Federal Institute of Technology Zurich, Zurich, Switzerland; Philips, Horgen, SwitzerlandInstitute for Biomedical Engineering, University and Swiss Federal Institute of Technology Zurich, Zurich, Switzerland; Zurich Center for Integrative Human Physiology, University of Zurich, Switzerland; Max Planck Institute for Biological Cybernetics, Tübingen, Germany; University of Texas Southwestern Medical Center, Dallas, TX, USACenter for Addictive Disorders, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Selnaustrasse 9, Zurich 8001, SwitzerlandDepartment of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology Zurich, SwitzerlandDepartment of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Switzerland; Zurich Center for Integrative Human Physiology, University of Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology Zurich, SwitzerlandCenter for Addictive Disorders, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Selnaustrasse 9, Zurich 8001, SwitzerlandCenter for Addictive Disorders, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Selnaustrasse 9, Zurich 8001, SwitzerlandTobacco smoking is one of the main causes of premature death worldwide and quitting success remains low, highlighting the need to understand the neurobiological mechanisms underlying relapse. Preclinical models have shown that the amygdala and glutamate play an important role in nicotine addiction. The aims of this study were to compare glutamate and other metabolites in the amygdala between smokers and controls, and between different smoking states. Furthermore, associations between amygdalar metabolite levels and smoking characteristics were explored.A novel non-water-suppressed proton magnetic resonance spectroscopy protocol was applied to quantify neurometabolites in 28 male smokers (≥15 cigarettes/day) and 21 non-smoking controls, matched in age, education, verbal IQ, and weekly alcohol consumption. Controls were measured once (baseline) and smokers were measured in a baseline state (1–3 h abstinence), during withdrawal (24 h abstinence) and in a satiation state (directly after smoking). Baseline spectroscopy data were compared between groups by independent t-tests or Mann-Whitney-U tests. Smoking state differences were investigated by repeated-measures analyses of variance (ANOVAs). Associations between spectroscopy data and smoking characteristics were explored using Spearman correlations.Good spectral quality, high anatomical specificity (98% mean gray matter) and reliable quantification of most metabolites of interest were achieved in the amygdala. Metabolite levels did not differ between groups, but smokers showed significantly higher glutamine levels at baseline than satiation. Glx levels were negatively associated with pack-years and smoking duration.In summary, this study provides first insights into the neurometabolic profile of the amygdala in smokers with high anatomical specificity. By applying proton magnetic resonance spectroscopy, neurometabolites in smokers during different smoking states and non-smoking controls were quantified reliably. A significant shift in glutamine levels between smoking states was detected, with lower concentrations in satiation than baseline. The negative association between Glx levels and smoking quantity and duration may imply altered glutamate homeostasis with more severe nicotine addiction.http://www.sciencedirect.com/science/article/pii/S105381192400020XAmygdalaGlutamateGlutamineMagnetic resonance spectroscopyNicotine addictionSmoking |
| spellingShingle | Colette A Steinegger Niklaus Zoelch Andreas Hock Anke Henning Etna JE Engeli Christopher R Pryce Erich Seifritz Marcus Herdener Lea M Hulka Neurometabolic profile of the amygdala in smokers assessed with 1H-magnetic resonance spectroscopy NeuroImage Amygdala Glutamate Glutamine Magnetic resonance spectroscopy Nicotine addiction Smoking |
| title | Neurometabolic profile of the amygdala in smokers assessed with 1H-magnetic resonance spectroscopy |
| title_full | Neurometabolic profile of the amygdala in smokers assessed with 1H-magnetic resonance spectroscopy |
| title_fullStr | Neurometabolic profile of the amygdala in smokers assessed with 1H-magnetic resonance spectroscopy |
| title_full_unstemmed | Neurometabolic profile of the amygdala in smokers assessed with 1H-magnetic resonance spectroscopy |
| title_short | Neurometabolic profile of the amygdala in smokers assessed with 1H-magnetic resonance spectroscopy |
| title_sort | neurometabolic profile of the amygdala in smokers assessed with 1h magnetic resonance spectroscopy |
| topic | Amygdala Glutamate Glutamine Magnetic resonance spectroscopy Nicotine addiction Smoking |
| url | http://www.sciencedirect.com/science/article/pii/S105381192400020X |
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