0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Original Investigation |

Large-Scale Brain Network Coupling Predicts Acute Nicotine Abstinence Effects on Craving and Cognitive Function

Caryn Lerman, PhD1; Hong Gu, PhD2; James Loughead, PhD1; Kosha Ruparel, MSE3; Yihong Yang, PhD2; Elliot A. Stein, PhD2
[+] Author Affiliations
1Center for Interdisciplinary Research on Nicotine Addiction, Department of Psychiatry, University of Pennsylvania, Philadelphia
2Intramural Research Program, National Institute on Drug Abuse, Baltimore, Maryland
3Brain Behavior Laboratory, Department of Psychiatry, University of Pennsylvania, Philadelphia
JAMA Psychiatry. 2014;71(5):523-530. doi:10.1001/jamapsychiatry.2013.4091.
Text Size: A A A
Published online

Importance  Interactions of large-scale brain networks may underlie cognitive dysfunctions in psychiatric and addictive disorders.

Objectives  To test the hypothesis that the strength of coupling among 3 large-scale brain networks—salience, executive control, and default mode—will reflect the state of nicotine withdrawal (vs smoking satiety) and will predict abstinence-induced craving and cognitive deficits and to develop a resource allocation index (RAI) that reflects the combined strength of interactions among the 3 large-scale networks.

Design, Setting, and Participants  A within-subject functional magnetic resonance imaging study in an academic medical center compared resting-state functional connectivity coherence strength after 24 hours of abstinence and after smoking satiety. We examined the relationship of abstinence-induced changes in the RAI with alterations in subjective, behavioral, and neural functions. We included 37 healthy smoking volunteers, aged 19 to 61 years, for analyses.

Interventions  Twenty-four hours of abstinence vs smoking satiety.

Main Outcomes and Measures  Inter-network connectivity strength (primary) and the relationship with subjective, behavioral, and neural measures of nicotine withdrawal during abstinence vs smoking satiety states (secondary).

Results  The RAI was significantly lower in the abstinent compared with the smoking satiety states (left RAI, P = .002; right RAI, P = .04), suggesting weaker inhibition between the default mode and salience networks. Weaker inter-network connectivity (reduced RAI) predicted abstinence-induced cravings to smoke (r = −0.59; P = .007) and less suppression of default mode activity during performance of a subsequent working memory task (ventromedial prefrontal cortex, r = −0.66, P = .003; posterior cingulate cortex, r = −0.65, P = .001).

Conclusions and Relevance  Alterations in coupling of the salience and default mode networks and the inability to disengage from the default mode network may be critical in cognitive/affective alterations that underlie nicotine dependence.

Figures in this Article

Sign in

Create a free personal account to sign up for alerts, share articles, and more.

Purchase Options

• Buy this article
• Subscribe to the journal

First Page Preview

View Large
First page PDF preview

Figures

Place holder to copy figure label and caption
Figure 1.
Functional Magnetic Resonance Images Demonstrating Results of Independent Component Analysis (ICA)

Four networks generated from group ICA of the resting state data were identified as the salience network (SN), default mode network (DMN), and left and right executive control network (ECN). Spatial maps were converted to z score images and then thresholded at z = 3.5 via a mixture model fit. Network maps are displayed in red-yellow overlaid onto the Talairach standard brain map based on neurological (left = left) convention. Slice coordinates are given in millimeters. The key SN regions included the dorsal anterior cingulate cortex (ACC)/paracingulate gyrus (Talairach coordinates: 3, 21, 33), bilateral anterior insula (left, −39, 9, 3; right, 51, 15, 0), dorsolateral prefrontal cortex (DLPFC) (left, −30, 45, 30; right, 30, 48, 30), supramarginal gyrus (left, −57, −45, 30; right, 57, −42, 33), and precuneus (12, −69, 36). Together, the left and right ECN covered the bilateral DLPFC (Talairach coordinates: left, −42, 45, 6; right, 45, 33, 25), parietal cortices (left, −39, −51, 42; right, 39, −57, 48), middle temporal gyrus (left, −51, −54, −9; right, 51, −57, −9), and dorsal medial frontal gyrus (left, −6, 27, 45; right, 6, 30, 45). The DMN included the posterior cingulate cortex (Talairach coordinates: 6, −57, 27), bilateral angular gyrus (left, −42, −69, 33; right, 48, −63, 30), ventromedial prefrontal cortex/rostral ACC (3, 54, 3), and temporal gyrus (left, −57, −9, −15; right, 60, −18, −15).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.
Resource Allocation Index (RAI) in the Abstinence vs Smoking States

Rendered brain figures present network components identified by group independent component analysis. Compared with the smoking state, the RAI for the left hemisphere (mL) decreased in abstinence (P = .002); the RAI for the right hemisphere (mR) showed a decreasing trend (P = .04). A thinner path connecting the salience network (SN) and executive control network (ECN) and the path connecting the SN and default mode network (DMN) in the abstinence (vs smoking) states illustrates decreased coupling between the networks. − Indicates negative correlation; +, positive correlation.aDifferences were significant.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.
Between-Network Coupling in the Abstinence vs Smoking States

Significant reduction in correlation between the salience network (SN) and default mode network (DMN) (P = .02) in the abstinence vs smoking states. LECN indicates left executive control network; RECN, right executive control network. Whiskers indicate SD.aDifferences were significant.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 4.
Resource Allocation Index (RAI) Correlation With Smoking Urge Score

Partial regression plots of the difference of brief Questionnaire on Smoking Urges score between the abstinence and smoking states (∆QSUa − s) against the difference of the RAI in the right hemisphere between states (∆mRa − s).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 5.
Resource Allocation Index (RAI) Correlations With Working Memory (WM) Task Activation

Partial regression plots of the difference between the abstinence vs smoking states of the WM task-induced blood oxygenation level–dependent change ([dS/S0]a − s) averaged across memory load in the ventromedial prefrontal cortex (A) and posterior cingulate cortex regions (B) against the difference of the RAI in the left hemisphere (∆mL,a − s). Markers indicate individual participants.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 6.
Schematic of Changes in the Association of the Resource Allocation Index (RAI) Between the Abstinence vs Smoking Sessions

Changes in the working memory (WM)–induced signal percentage change between states (dS/S)a − s, the RAI in the right and left hemispheres between states (∆mR,a − s and ∆mL,a − s, respectively), and the brief Questionnaire on Smoking Urges (QSU) score between states (∆QSUa − s) are depicted. PCC indicates posterior cingulate cortex; VMPFC, ventromedial prefrontal cortex. Upward arrow indicates increase; downward arrows, decrease.

Graphic Jump Location

Tables

References

Correspondence

CME
Also Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
Please click the checkbox indicating that you have read the full article in order to submit your answers.
Your answers have been saved for later.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
Submit a Comment

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Web of Science® Times Cited: 3

Sign in

Create a free personal account to sign up for alerts, share articles, and more.

Purchase Options

• Buy this article
• Subscribe to the journal

Related Content

Customize your page view by dragging & repositioning the boxes below.

See Also...
Articles Related By Topic
Related Collections
PubMed Articles
Jobs
JAMAevidence.com
brightcove.createExperiences();