Factors modulating neural reactivity to drug cues in addiction: A survey of human neuroimaging studies

doi:10.1016/j.neubiorev.2013.10.013

Neuroscience & Biobehavioral Reviews

Volume 38, January 2014, Pages 1-16

https://doi.org/10.1016/j.neubiorev.2013.10.013 Get rights and content

Highlights

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Neural reactivity to cocaine, alcohol and tobacco cues is modulated by:.
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Treatment status, length and intensity of use, addiction severity, abstinence.
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Stress, drug availability, sensory modality and length of presentation of cues.
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Explicit and implicit cognitive regulation.
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These factors have both main and interactive effects.

Abstract

Human neuroimaging studies suggest that neural cue reactivity is strongly associated with indices of drug use, including addiction severity and treatment success. However, little is known about factors that modulate cue reactivity. The goal of this review, in which we survey published fMRI and PET studies on drug cue reactivity in cocaine, alcohol, and tobacco cigarette users, is to highlight major factors that modulate brain reactivity to drug cues. First, we describe cue reactivity paradigms used in neuroimaging research and outline the brain circuits that underlie cue reactivity. We then discuss major factors that have been shown to modulate cue reactivity and review specific evidence as well as outstanding questions related to each factor. Building on previous model-building reviews on the topic, we then outline a simplified model that includes the key modulatory factors and a tentative ranking of their relative impact. We conclude with a discussion of outstanding challenges and future research directions, which can inform future neuroimaging studies as well as the design of treatment and prevention programs.

Introduction

Growing evidence suggests that drug cue reactivity, as assessed with functional MRI (fMRI), positron emission tomography (PET), and related neuroimaging techniques, as well as behavioral and autonomic measures, is strongly associated with a number of indices of drug use, including addiction severity and treatment success. However, factors that modulate cue reactivity remain incompletely understood and in some cases the direction of causal influence unclear, impeding a translation of this knowledge to clinical practice. Therefore, our goal in this review is to identify and characterize major factors that modulate brain reactivity to drug cues, which may inform future neuroimaging studies as well as the design, selection, and tailoring of treatment and prevention programs. Toward that goal, we survey published fMRI and PET studies on drug cue reactivity in cocaine, alcohol, and tobacco cigarette users, with the focus on identifying and characterizing specific factors that modulate this reactivity. We first describe cue reactivity paradigms used in human neuroimaging research and outline the brain circuits that underlie drug cue reactivity. We then discuss major factors that have been shown to modulate cue reactivity and review specific evidence as well as outstanding questions related to each factor. In light of recent findings, we highlight the importance of implicit and explicit cognitive regulation over drug cue reactivity and the conditioned drug-seeking behavioral responses that these cues engender. Building on previous model-based reviews (Field and Cox, 2008, Franken, 2003, Wilson et al., 2004), we then provide a simplified model that includes the key modulatory factors and offer a tentative ranking of their relative impact on neural drug-cue reactivity in drug users. We conclude with a discussion of outstanding challenges and future research directions.

Section snippets

Drug cue reactivity paradigms in human neuroimaging research

A number of different neuroimaging paradigms have been used to investigate the neural correlates of drug cue reactivity in human drug users. The shared feature of these paradigms is that drug users are exposed to stimuli associated with their respective drug of abuse. These drug-related cues may be visual (seeing words, pictures or silent videos) (Janes et al., 2010, Luijten et al., 2011), auditory (e.g., listening to imagery scripts) (Kilts et al., 2001, Seo et al., 2011), audiovisual (

Mesocorticolimbic system and brain circuits of reward, motivation, and goal-directed behavior

A common characteristic, and arguably a shared neurobiological mechanism, of most if not all drugs of abuse is that they increase extracellular dopamine (DA) concentration in the mesocorticolimbic system, including the ventral striatum (VS), extended amygdala, hippocampus, anterior cingulate (ACC), prefrontal cortex (PFC), and insula, which are innervated by dopaminergic projections predominantly from the ventral tegmental area (VTA) (Hyman et al., 2006, Nestler, 2005). Such directly or

Addiction severity, craving, and treatment outcome

The clinical relevance of drug cue reactivity is well documented by behavioral studies (Field and Cox, 2008). Drug cue reactivity is associated with, and in some cases predictive of, a number of clinical measures of drug use and dependence, including length and intensity of drug use, addiction severity, risk of relapse, treatment outcomes, and use-associated problems. However, it should be emphasized that the direction of influence, or cause and effect, are less clear. On the one hand, chronic

Abstinence and withdrawal symptoms

Abstinence and associated withdrawal symptoms (including irritable, anxious, or depressed mood, difficulty concentrating, motor disturbances, disturbances in appetite and sleep, as well as changes in heart rate, blood pressure, and body temperature) are also likely to modulate neural reactivity to drug cues in drug users. Craving for a drug is sometimes considered a symptom of drug withdrawal as well. In fact, drug seeking during abstinence-induced withdrawal has been postulated to be at least

Sensory modality and length of presentation of drug cues

The sensory modality of the cues can also influence the behavioral and brain cue reactivity itself. Behavioral experiments have demonstrated pronounced differences in the ability of drug cues to elicit behavioral and psychophysiological reactions depending on the sensory modality (Johnson et al., 1998, Reid et al., 2006, Shadel et al., 2001, Wray et al., 2011). For instance, a recent fMRI study revealed that haptic smoking cues activate the DS more strongly than visual smoking cues (Yalachkov

Explicit and implicit regulation of drug cue reactivity

Current theories of addiction posit that, with repeated drug use and associated DA processes in the mesocorticolimbic and nigrostriatal circuits, drug-related cues acquire incentive-motivational salience, which gives them the capacity to trigger craving and drug seeking (Robinson and Berridge, 1993). In the process, drug cues also acquire attentional salience, which is manifested as a powerful attentional bias for drug cues in drug-dependent individuals (Field and Cox, 2008, Franken, 2003; see

Stressor exposure

Stressor exposure is known to interact with drug-related cues as a potent trigger of craving and relapse to drug-taking behavior following abstinence (for reviews, see Koob, 2008, Sinha, 2008). Stressors and drug-related cues also engage partially overlapping brain systems, including the mesocorticolimbic system (for review, see Sinha and Li, 2007). Therefore, stressor exposure would be expected to impact neural reactivity to drug cues in drug users. Consistent with this view, when a

Toward an integrative model of neural reactivity to drug cues

As discussed in the sections above, human neuroimaging literature strongly suggests that the neural reactivity to drug cues is modulated by a number of both individual-specific and study-specific factors. Furthermore, these factors are likely to have both main and interactive effects, although the direction and magnitude of this modulation is not always well understood. To facilitate progress toward such understanding, we present a table summarizing our findings (see Table 1) and outline a

Outstanding challenges and future directions

Neural reactivity to drug cues has been proposed to be a key manifestation of addiction processes and may constitute a biomarker of addiction severity, treatment outcome, and risk of relapse. Yet considerable variability in the extensive neuroimaging literature on drug-cue reactivity has hindered translation of this knowledge to diagnosis, treatment, and prevention. This variability suggests that neural cue reactivity in drug users may be modulated by other factors, including both

Acknowledgements

A.J.J. and E.A.S. are supported by the National Institute on Drug Abuse Intramural Research Program (NIDA-IRP). M.J.N., J.K. and Y.Y. are supported by the Hessisches Ministerium für Wissenschaft und Kultur (LOEWE Forschungsschwerpunkt Neuronale Koordination Frankfurt).

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Published by Elsevier Ltd.

ReviewFactors modulating neural reactivity to drug cues in addiction: A survey of human neuroimaging studies

Highlights

Abstract

Introduction

Section snippets

Drug cue reactivity paradigms in human neuroimaging research

Mesocorticolimbic system and brain circuits of reward, motivation, and goal-directed behavior

Addiction severity, craving, and treatment outcome

Abstinence and withdrawal symptoms

Sensory modality and length of presentation of drug cues

Explicit and implicit regulation of drug cue reactivity

Stressor exposure

Toward an integrative model of neural reactivity to drug cues

Outstanding challenges and future directions

Acknowledgements

Neuron

Behav. Brain Res.

Neuropsychopharmacology

Biol. Psychiatry

Cortex

Curr. Biol.

Neuroimage

Biol. Psychiatry

Brain Res.

Drug Alcohol Depend.

Brain Res. Cogn. Brain Res.

Brain Res.

Biol. Psychiatry

Neuroimage

Neuroscience

Neuropsychopharmacology

Neuron

Neuroimage

Neurosci. Biobehav. Rev.

Drug Alcohol Depend.

Prog. Neuropsychopharmacol. Biol. Psychiatry

Biol. Psychol.

Neuroimage

Neuropsychologia

Eur. J. Pharmacol.

Biol. Psychiatry

Prog. Neurobiol.

Addict. Behav.

Trends Cogn. Sci.

Neuron

Neuron

Neurosci. Biobehav. Rev.

Neuroimage

Neuron

Brain Res. Brain Res. Rev.

Exposure to smoking cues during an emotion recognition task can modulate limbic fMRI activation in cigarette smokers

Addict. Biol.

Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective

Nat. Neurosci.

Effect of brain structure, brain function, and brain connectivity on relapse in alcohol-dependent patients

Arch. Gen. Psychiatry

Alcohol-associated stimuli activate the ventral striatum in abstinent alcoholics

Journal of Neural Transmission (Vienna, Austria: 1996)

Brain metabolic changes during cigarette craving

Arch. Gen. Psychiatry

Does erotic stimulus presentation design affect brain activation patterns? Event-related vs. blocked fMRI designs

Behav. Brain Funct.

Nicotinic excitation of rate ventral tegmental neurons in vitro studies by intracellular recording

Br. J. Pharmacol.

Action observation and acquired motor skills: an FMRI study with expert dancers

Cereb. Cortex

Prelude to passion: limbic activation by “unseen” drug and sexual cues

PLoS One

Limbic activation during cue-induced cocaine craving

Am. J. Psychiatry

Identifying neurobiological phenotypes associated with alcohol use disorder severity

Neuropsychopharmacology

Neural responses associated with cue-reactivity in frequent cannabis users

Addict. Biol.

Interoception: the sense of the physiological condition of the body

Curr. Opin. Neurobiol.

Influence of alcohol use and family history of alcoholism on neural response to alcohol cues in college drinkers

Alcohol. Clin. Exp. Res.

Effects of acute nicotine abstinence on cue-elicited ventral striatum/nucleus accumbens activation in female cigarette smokers: a functional magnetic resonance imaging study

Brain Imaging Behav.

Review
Factors modulating neural reactivity to drug cues in addiction: A survey of human neuroimaging studies