Nicotine Abstinence Influences the Calculation of Salience in Discrete Insular Circuits

Fedota, John R.; Ding, Xiaoyu; Matous, Allison L.; Salmeron, Betty Jo; McKenna, Michael R.; Gu, Hong; Ross, Thomas J.; Stein, Elliot A.

doi:10.1016/j.bpsc.2017.09.010

Cited by 43 publications

(50 citation statements)

References 83 publications

(109 reference statements)

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“…Rather than a blanket inability to engage cognitive and attentional resources, the deficit appears specific to conditions where only relatively minimal attention is required. The robust effects 14 on attention that we report are in line with literature on attention-enhancing effects of nicotine 14,41 and problems with sustained attention in smokers [42][43][44][45] .…”

Section: Discussionsupporting

confidence: 89%

Nicotine dependence (trait) and acute nicotinic stimulation (state) modulate attention but not cognitive control: converging fMRI evidence from Go-Nogo and Flanker tasks

Lesage

Sutherland

Ross

et al. 2019

Preprint

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Cognitive deficits during nicotine withdrawal may contribute to smoking relapse. However, interacting effects of chronic nicotine dependence and acute nicotine withdrawal on cognitive control are poorly understood. Here, we examine the effects of nicotine dependence (trait; smokers versus non-smoking controls), and acute nicotinic stimulation (state; administration of nicotine and varenicline, two FDAapproved smoking cessation aids, during abstinence), on two well-established tests of cognitive control, the Go-Nogo task and the Flanker task, during fMRI scanning. We compared performance and neural responses between these four pharmacological manipulations in a double-blind, placebo-controlled crossover design. As expected, performance in both tasks was modulated by nicotine dependence, abstinence and pharmacological manipulation. However, effects were driven entirely by conditions that required less cognitive control. When demand for cognitive control was high, abstinent smokers showed no deficits. By contrast, acutely abstinent smokers showed performance deficits in easier conditions and missed more trials. Go-Nogo fMRI results showed decreased inhibition-related neural activity in right anterior insula and right putamen in smokers and decreased dorsal anterior cingulate cortex activity on nicotine across groups. No effects were found on inhibition-related activity during the Flanker task, or on error-related activity in either task. Given robust nicotinic effects on physiology and behavioral deficits in attention, we are confident that pharmacological manipulations were effective. Thus, findings fit a recent proposal that abstinent smokers show decreased ability to divert cognitive resources at low or intermediate cognitive demand, while performance at high cognitive demand remains relatively unaffected, suggesting a primary attentional deficit during acute abstinence.

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Section: Discussionsupporting

confidence: 89%

Nicotine dependence (trait) and acute nicotinic stimulation (state) modulate attention but not cognitive control: converging fMRI evidence from Go-Nogo and Flanker tasks

Lesage

Sutherland

Ross

et al. 2019

Preprint

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“…SUD studies consistently report a reduction in TVC associated with SUD, including a study from our lab reporting decreases in TVC as a function of acute nicotine abstinence 45 .…”

Section: Introductionmentioning

confidence: 75%

“…Thus, we predict that the external perturbations of and stress induced by acute abstinence in SUD will be associated with reduced TVC.To date most TVC studies have interrogated data from healthy individuals, and demonstrate reductions in TVC associated with poorer behavioral performance 31,38-40 and increased negative affect 41 . Consistent with these affective and behavioral disruptions, a small but growing literature on SUD-related change in dynamic TVC has begun to appear [42][43][44][45] . These…”

mentioning

confidence: 96%

Time varying connectivity across the brain changes as a function of nicotine abstinence state

Fedota

Ross

Castillo

et al. 2020

Preprint

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Background:The Nicotine Withdrawal Syndrome (NWS) includes affective and cognitive disruptions whose incidence and severity vary across time during acute abstinence. However, most network-level neuroimaging employs static measures of resting state functional connectivity (rsFC), assuming time-invariance, and unable to capture dynamic brain-behavior relationships. Recent advances in rsFC signal processing allow characterization of "time varying connectivity" (TVC), which characterizes network communication between sub-networks that reconfigure over the course of data collection. As such, TVC may more fully describe network dysfunction related to the NWS. Methods:To isolate alterations in the frequency and diversity of communication across network boundaries as a function of acute nicotine abstinence we scanned cigarette smokers in the nicotine sated and abstinent states and applied a previously-validated method to characterize TVC at a network and nodal level within the brain. Results:During abstinence, we found brain wide decreases in the frequency of interactions between network nodes in different modular communities (i.e. temporal flexibility; TF). In addition, within a subset of the networks examined the variability of these interactions across community boundaries (i.e. spatiotemporal diversity; STD) also decreased. Finally, within two of these networks the decrease in STD was significantly related to NWS clinical symptoms. Conclusions:Employing multiple measures of TVC in a within subjects' design, we characterized a novel set of changes in network communication and link these changes to specific behavioral symptoms of the NWS. These reductions in TVC provide a meso-scale network description of the relative inflexibility of specific large-scale brain networks as a result of acute abstinence. Acute nicotine abstinence is a key early hurdle to smoking cessation as most cessation attempts fail within a week of their target quit day 1 . These poor treatment outcomes are due, in part, to components of the Nicotine Withdrawal Syndrome (NWS) precipitated by acute smoking abstinence. The aversive symptoms of the NWS both dissuade smokers from attempting to quit 2 and promote relapse via negative reinforcement-the relief of the withdrawal state 3-5 .The clinical presentation of the NWS includes increases in negative affect 6,7 , lapses of attention [8][9][10][11] , and punctate craving for nicotine 6 . Critically, across both subjective and objective measures of NWS symptoms, variability in onset, time course, and phenomenology is consistently observed 12-17 . For example, craving increases early and again late in the day 15 , and negative affect spikes intermittently following cessation 17 . Symptoms are more variable in withdrawn smokers after quitting than before, suggesting that smoking may buffer or constrain aversive symptoms, which are then "unleashed" by cessation 18 . The incidence of these NWS symptoms increases with increased acute psychosocial stress [19][20][21][22] . The volatility in affective disrupti...

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“…The MRI images in the present study were acquired in satiated state. As mentioned in our previous paper (Shen et al ., ), acute nicotine effects on functional circuits may be a function of circuits, resulting in decreased functional connectivity, increased functional connectivity or no effect (Hong et al ., ; Sutherland et al ., ; Fedota et al ., ). As such, it is possible that the four different functional circuits have their own FCS patterns.…”

Section: Discussionmentioning

confidence: 97%

Interactions between monoamine oxidase A rs1137070 and smoking on brain structure and function in male smokers

Shen

Huang

Wang

et al. 2018

Eur J of Neuroscience

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The monoamine oxidase A (MAOA) enzyme metabolizes monoamine neurotransmitters such as dopamine, serotonin and norepinephrine, and its genetic polymorphism (rs1137070) influences its activity level and is associated with smoking behaviors. However, the underlying neural mechanisms of the gene × environment interactions remain largely unknown. In this study, we aimed to explore the interactive effects of the rs1137070 and cigarette smoking on gray matter volume (GMV) and functional connectivity strength (FCS). A total of 81 smokers and 42 nonsmokers were enrolled in the present study. Voxel‐based morphometry analysis showed a significant rs1137070 genotype × smoking effect on the GMV of the left orbitofrontal cortex (OFC), such that individuals with risk allele had greater GMV among nonsmokers but not smokers. Meanwhile, rs1137070 variant and nicotine dependence interactively altered the FCS of the right hippocampus, the left inferior parietal lobule (IPL), the left dorsolateral prefrontal cortex and bilateral OFC. In addition, the FCS in the left IPL was correlated with smoking initiation and smoking years in smokers with the risk allele. These findings suggest that MAOA rs1137070 contributes to the susceptibility to nicotine dependence through its influence on brain circuits involved in reward and attention, and interacts with smoking in the progression.

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Nicotine Abstinence Influences the Calculation of Salience in Discrete Insular Circuits

Cited by 43 publications

References 83 publications

Nicotine dependence (trait) and acute nicotinic stimulation (state) modulate attention but not cognitive control: converging fMRI evidence from Go-Nogo and Flanker tasks

Nicotine dependence (trait) and acute nicotinic stimulation (state) modulate attention but not cognitive control: converging fMRI evidence from Go-Nogo and Flanker tasks

Time varying connectivity across the brain changes as a function of nicotine abstinence state

Interactions between monoamine oxidase A rs1137070 and smoking on brain structure and function in male smokers

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