Combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophrenia
The smoking rate is high in patients with schizophrenia. Brain stimulation targeting conventional brain circuits associated with nicotine addiction has also yielded mixed results. We aimed to identify alternative circuitries associated with nicotine addiction in both the general population and schiz...
| Main Authors: | , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2024-03-01
|
| Series: | Brain Stimulation |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1935861X24000354 |
| _version_ | 1797262903098736640 |
|---|---|
| author | Xiaoming Du Fow-Sen Choa Joshua Chiappelli Heather Bruce Mark Kvarta Ann Summerfelt Yizhou Ma William T. Regenold Kevin Walton George F. Wittenberg Stephanie Hare Si Gao Andrew van der Vaart Zhiwei Zhao Shuo Chen Peter Kochunov L. Elliot Hong |
| author_facet | Xiaoming Du Fow-Sen Choa Joshua Chiappelli Heather Bruce Mark Kvarta Ann Summerfelt Yizhou Ma William T. Regenold Kevin Walton George F. Wittenberg Stephanie Hare Si Gao Andrew van der Vaart Zhiwei Zhao Shuo Chen Peter Kochunov L. Elliot Hong |
| author_sort | Xiaoming Du |
| collection | DOAJ |
| description | The smoking rate is high in patients with schizophrenia. Brain stimulation targeting conventional brain circuits associated with nicotine addiction has also yielded mixed results. We aimed to identify alternative circuitries associated with nicotine addiction in both the general population and schizophrenia, and then test whether modulation of such circuitries may alter nicotine addiction behaviors in schizophrenia. In Study I of 40 schizophrenia smokers and 51 non-psychiatric smokers, cross-sectional neuroimaging analysis identified resting state functional connectivity (rsFC) between the dorsomedial prefrontal cortex (dmPFC) and multiple extended amygdala regions to be most robustly associated with nicotine addiction severity in healthy controls and schizophrenia patients (p = 0.006 to 0.07). In Study II with another 30 patient smokers, a proof-of-concept, patient- and rater-blind, randomized, sham-controlled rTMS design was used to test whether targeting the newly identified dmPFC location may causally enhance the rsFC and reduce nicotine addiction in schizophrenia. Although significant interactions were not observed, exploratory analyses showed that this dmPFC–extended amygdala rsFC was enhanced by 4-week active 10Hz rTMS (p = 0.05) compared to baseline; the severity of nicotine addiction showed trends of reduction after 3 and 4 weeks (p ≤ 0.05) of active rTMS compared to sham; Increased rsFC by active rTMS predicted reduction of cigarettes/day (R = −0.56, p = 0.025 uncorrected) and morning smoking severity (R = −0.59, p = 0.016 uncorrected). These results suggest that the dmPFC–extended amygdala circuit may be linked to nicotine addiction in schizophrenia and healthy individuals, and future efforts targeting its underlying pathophysiological mechanisms may yield more effective treatment for nicotine addiction. |
| first_indexed | 2024-04-25T00:04:30Z |
| format | Article |
| id | doaj.art-19a62d0c0d86446e9e5578dccda7a876 |
| institution | Directory Open Access Journal |
| issn | 1935-861X |
| language | English |
| last_indexed | 2024-04-25T00:04:30Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Brain Stimulation |
| spelling | doaj.art-19a62d0c0d86446e9e5578dccda7a8762024-03-14T06:14:25ZengElsevierBrain Stimulation1935-861X2024-03-01172324332Combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophreniaXiaoming Du0Fow-Sen Choa1Joshua Chiappelli2Heather Bruce3Mark Kvarta4Ann Summerfelt5Yizhou Ma6William T. Regenold7Kevin Walton8George F. Wittenberg9Stephanie Hare10Si Gao11Andrew van der Vaart12Zhiwei Zhao13Shuo Chen14Peter Kochunov15L. Elliot Hong16Louis A. Faillace Department of Psychiatry and Behavioral Sciences at McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX, USA; Corresponding author.Department of Electrical Engineering and Computer Science, University of Maryland Baltimore County, Baltimore, MD, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USALouis A. Faillace Department of Psychiatry and Behavioral Sciences at McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX, USANoninvasive Neuromodulation Unit, Experimental Therapeutics and Pathophysiology Branch, Division of Intramural Research Program, National Institute of Mental Health, National Institutes of Health, NIH Clinical Center, Bethesda, MD, USAClinical Research Grants Branch, Division of Therapeutics and Medical Consequences, National Institute on Drug Abuse, National Institutes of Health, Bethesda, MD, USAHuman Engineering Research Laboratories, VA RR&D Center of Excellence, VA Pittsburgh Healthcare System, Pittsburgh, PA, USA; Rehabilitation Neural Engineering Laboratories, University of Pittsburgh, Pittsburgh, PA, USA; Department of Neurology, University of Pittsburgh, Pittsburgh, PA, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USALouis A. Faillace Department of Psychiatry and Behavioral Sciences at McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USADepartment of Mathematics, University of Maryland, College Park, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USALouis A. Faillace Department of Psychiatry and Behavioral Sciences at McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX, USALouis A. Faillace Department of Psychiatry and Behavioral Sciences at McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX, USAThe smoking rate is high in patients with schizophrenia. Brain stimulation targeting conventional brain circuits associated with nicotine addiction has also yielded mixed results. We aimed to identify alternative circuitries associated with nicotine addiction in both the general population and schizophrenia, and then test whether modulation of such circuitries may alter nicotine addiction behaviors in schizophrenia. In Study I of 40 schizophrenia smokers and 51 non-psychiatric smokers, cross-sectional neuroimaging analysis identified resting state functional connectivity (rsFC) between the dorsomedial prefrontal cortex (dmPFC) and multiple extended amygdala regions to be most robustly associated with nicotine addiction severity in healthy controls and schizophrenia patients (p = 0.006 to 0.07). In Study II with another 30 patient smokers, a proof-of-concept, patient- and rater-blind, randomized, sham-controlled rTMS design was used to test whether targeting the newly identified dmPFC location may causally enhance the rsFC and reduce nicotine addiction in schizophrenia. Although significant interactions were not observed, exploratory analyses showed that this dmPFC–extended amygdala rsFC was enhanced by 4-week active 10Hz rTMS (p = 0.05) compared to baseline; the severity of nicotine addiction showed trends of reduction after 3 and 4 weeks (p ≤ 0.05) of active rTMS compared to sham; Increased rsFC by active rTMS predicted reduction of cigarettes/day (R = −0.56, p = 0.025 uncorrected) and morning smoking severity (R = −0.59, p = 0.016 uncorrected). These results suggest that the dmPFC–extended amygdala circuit may be linked to nicotine addiction in schizophrenia and healthy individuals, and future efforts targeting its underlying pathophysiological mechanisms may yield more effective treatment for nicotine addiction.http://www.sciencedirect.com/science/article/pii/S1935861X24000354Nicotine addictionSchizophreniaSmokingTMSConnectivityImaging |
| spellingShingle | Xiaoming Du Fow-Sen Choa Joshua Chiappelli Heather Bruce Mark Kvarta Ann Summerfelt Yizhou Ma William T. Regenold Kevin Walton George F. Wittenberg Stephanie Hare Si Gao Andrew van der Vaart Zhiwei Zhao Shuo Chen Peter Kochunov L. Elliot Hong Combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophrenia Brain Stimulation Nicotine addiction Schizophrenia Smoking TMS Connectivity Imaging |
| title | Combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophrenia |
| title_full | Combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophrenia |
| title_fullStr | Combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophrenia |
| title_full_unstemmed | Combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophrenia |
| title_short | Combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophrenia |
| title_sort | combining neuroimaging and brain stimulation to test alternative causal pathways for nicotine addiction in schizophrenia |
| topic | Nicotine addiction Schizophrenia Smoking TMS Connectivity Imaging |
| url | http://www.sciencedirect.com/science/article/pii/S1935861X24000354 |
| work_keys_str_mv | AT xiaomingdu combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT fowsenchoa combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT joshuachiappelli combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT heatherbruce combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT markkvarta combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT annsummerfelt combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT yizhouma combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT williamtregenold combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT kevinwalton combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT georgefwittenberg combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT stephaniehare combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT sigao combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT andrewvandervaart combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT zhiweizhao combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT shuochen combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT peterkochunov combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia AT lelliothong combiningneuroimagingandbrainstimulationtotestalternativecausalpathwaysfornicotineaddictioninschizophrenia |