Trends in Cognitive Sciences
OpinionThe Neurocircuitry of Impaired Insight in Drug Addiction☆
Introduction
Based on the latest report from the US Department of Health and Human Services, only 4.5% of the 21.1 million persons classified in 2006 as needing, but not receiving, substance use treatment, reported a perceived need for therapy [1]. Therefore, one of the greatest problems in drug addiction treatment is that the individuals who require treatment do not even recognize the need for therapeutic help. This treatment resistance could reflect in part both the failure of society to recognize addiction as a disease, and the blame and repudiation placed on the afflicted individuals. We propose here that this impairment might also reflect dysfunction of the neural circuits underlying interoception, self-awareness, and appropriate social, emotional and cognitive responses. Understanding these neuronal circuits could improve therapeutic strategies for treating addiction.
Interoception, self-awareness, and consciousness are interrelated concepts, collectively used to illustrate the ability to recognize and describe one's own (and others’) behaviors, cognitions and mental states (see Box 1: What is insight?). Dysfunctional insight characterizes various neuropsychiatric disorders, spanning classic neurological insults (e.g. causing visual neglect or anosognosia for hemiplegia) to classic psychiatric disorders (e.g. schizophrenia, mania and other mood disorders), as recently reviewed [2]. In brief, impaired awareness in these disorders can take the form of failure to recognize an illness, denial of illness, compromised control of action and unawareness of the patient's social incompetence. Although seemingly disparate, the signs and symptoms of impaired awareness in these disorders have been organized into coherent theoretical frameworks. These models primarily highlight internal representations (of the actual, desired and predicted states of our own body and external world) [3] that possibly utilize the dynamic interactions of specialized component processes via a distributed neural network [4]. Damage to specific sets of neural circuits might interrupt the internal signals that indicate a problem. Thus, the absence of information about the left side of one's body is no more worrisome than lack of visual information from behind one's head - no impairment is registered because no such input is expected [4]. An intact interpretive process continues to supply explanations that seem self-evident, even when exceedingly wrong [4] (e.g. ‘I am not using my left hand, not because it is paralyzed but because someone is preventing me from using it’).
In the current opinion article, we argue that as a cognitive disorder [5], drug addiction might share with these neuropsychiatric disorders similar abnormalities in self-awareness and behavioral control that can be attributed to an underlying neural dysfunction. These commonalities could include a dissociation between self-report and behavior. Thus, forced-choice behavior (e.g. choice between two alternatives) might indicate non-random behavior whereas the spontaneous attempt to explain this behavior could be compromised or lacking. Specifically, similar to blind-sightedness, where patients report they cannot see the visual cues that actually guide their behavior [6], one could conceptualize drug addiction as a compromised ability to recognize external and internal drug-related cues. Such attenuated awareness of these cues might lead to the false belief that one is in control over drug taking behavior. An associated lack of recognition that one is afflicted by a disease or an underestimation of the severity of illness in drug addiction might drive these individuals’ excessive drug use, where control of use becomes exceedingly dysregulated.
Consistent with this view, there is some appreciation of altered awareness as part of the diagnosis of drug dependence in the Diagnostic and Statistical Manual of Mental Disorders, the main consensus criteria for psychiatric diagnosis, where emphasis is placed on continued drug use despite knowledge of negative consequences. Indeed, only a minority of heavy drinkers define their own drinking as problematic even in the face of acknowledged negative consequences [7]. It is also well known that self-reported (conscious) craving is a poor predictor of relapse [8]. We recently reported a discordance between self-reported motivation and goal-driven behavior in cocaine addicted individuals [9] as illustrated by the forced-choice results depicted in Figure 1[10]. This discordance is mirrored by brain-behavior dissociations in tasks of reward processing [11], behavioral monitoring and emotional suppression [12]. This internal discordance (self-report vs. behavior or brain-behavior) can be validated by a discrepancy between the patients’ self-report and informants’ reports (e.g. by a family member or a treatment provider) [13]; correlations with neuropsychological performance [14] support the notion that neurocognitive dysfunction underlies such compromised self-awareness, frequently mislabeled as “denial” (which assumes a priori knowledge, and intent to negate or minimize, the severity of symptoms).
Although drug addiction might also share with the other neuropsychiatric disorders a resistance to evidence-based or cognitively-driven changes in self-awareness [4], self-awareness enhancements might improve treatment outcome possibly through impact on select neuropsychological functions (e.g. enhancing accuracy of self-report [15], motivation or sense of agency [16]). For example, higher risk awareness (of the link between cigarette smoking and heart disease) was associated with a self-reported desire to reduce smoking in a very large sample of young adults [17]. In addition, better awareness of severity of alcohol use predicted actual abstinence for up to one year after treatment in 117 male alcoholics [18]. Nevertheless, self-awareness enhancements could also increase the salience of negative affect [15], which might lead to increased drug use to alleviate the associated negative affective state. Thus, modulating self-awareness needs to be well monitored and expertly supervised, especially in addicted individuals with comorbid psychiatric disorders. An example for the interaction between baseline self-awareness and alcohol use in response to negative reinforcement is provided in Box 2: Self-awareness and alcohol.
Given that self-awareness and interoception seem crucial to understanding drug addiction and its treatment, here we review their putative underlying neural circuits. Abnormalities in the insula and medial regions of the prefrontal cortex (which include the anterior cingulate and mesial orbitofrontal cortices), and in subcortical regions (including the striatum), have been highlighted when comparing drug addicted individuals with neurological patients with focal brain damage [19]. These same corticolimbic brain regions have been associated with interoception and behavioral control, and with interrelated functions (habit formation and valuation), as reviewed below. These considerations expand the conceptualization of addiction beyond its association with the reward circuit, neurocognitive impairments in response inhibition and salience attribution [5] and neuroadaptations in memory circuits [20], to include compromised interoception, self-awareness and insight into illness.
Section snippets
Interoception and behavioral control: Unique and conjoint roles for the insula and anterior cingulate cortices
The posterior insula in primates contains interoceptive representation of the physiological condition of the body [21]. This activity is integrated in the middle insula with salient activity from all sensory and sensorimotor pathways, from homeostatic forebrain structures (amygdala, hypothalamus), and from systems concerned with reward and salience processing (ventral striatum) [21]. The anterior insula of humans further integrates emotionally salient activity from other forebrain regions,
Insula and anterior cingulate roles in drug addiction
A recent study explored the role of insula damage in addiction [40]. In a retrospective design assessing changes in cigarette smoking after brain damage, 19 smokers who sustained damage in the insula were compared with 50 smokers who sustained damage in other brain areas. Results revealed that smokers with brain damage involving the insula were significantly (more than 100 times) more likely than smokers with brain damage not involving the insula to undergo a ‘disruption of smoking addiction’,
Other regions and processes implicated in awareness in drug addiction
An influential theoretical account has posited that the ‘switch’ from voluntary drug use to habitual and progressively compulsive drug use represents a transition at the neural level from prefrontal cortical to striatal control over drug-seeking and drug-taking behaviors, as well as a progression from ventral to more dorsal domains of the striatum, mediated at least in part by its stratified dopaminergic innervation (see review [51]). Specifically, lateral parts of the dorsal striatum - the
Drug-related stimuli outside awareness activate brain motivational circuits and predict future positive affect to visible drug cues
Conscious drug desire is a hallmark feature of the addictions [59]. Afflicted individuals can sometimes identify stimuli that preceded the desire state: “I was OK until I suddenly saw an old broken crack (cocaine) pipe in the gutter; then the craving hit me…”. Often, however, users are unaware of triggers: “Doc, I really don’t know what happened. One minute I was OK, and the next second the craving hit me, and I was off on a mission to get the drug…”. ‘Volcanic’ craving that erupts suddenly
Treatment implications
Motivational interviewing is a frequent intervention in drug abuse treatment used to enhance the readiness for change and to maintain that change. However, cue-triggered appetitive motivation that begins almost instantly, outside awareness, might not be amenable to such an insight-oriented approach and indeed deterioration over time in the effectiveness of insight-oriented psychotherapies in addicted individuals has been documented [63]. Alternative interventions might include cognitive
Summary and future directions
Here we put forth the argument that insight and awareness are compromised in drug addicted individuals as possibly related to an underlying neural dysfunction in the brain regions that modulate interoception, behavioral monitoring, self-evaluation, and habit formation. However, direct empirical evidence for such impairment in drug addiction is scarce. Our major aim is therefore to call for future scientific exploration of the neural basis of insight and awareness in addiction. Tractable and
Conflicts of Interest Statement
Rita Goldstein consulted for Medical Directions, Inc. She has also received honoraria for speaking at seminars on Law and Neuroscience, co-sponsored by the Federal Judicial Center, Gruter Institute for Law and Behavioral Research, New York University, and the Catherine T. and John D. MacArthur Foundation Law & Neuroscience Project. Martin Paulus has consulted for Sepracor, Roche, and GSK and has received grant support from these pharmaceutical companies.
Acknowledgements/funding
The contribution of Steven J. Grant, Division of Clinical Neuroscience and Behavioral Research, National Institute on Drug Abuse, who reviewed and edited this manuscript is gratefully acknowledged. This manuscript is based on the symposium ‘Functional Neuroimaging Evidence for a Brain Network Underlying Impaired Insight Into Illness in Drug Addiction’ chaired by RZG and co-chaired by SJG at the 2008 annual meeting of the Society for Neuroscience, Washington DC. The preparation of this
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This manuscript has been authored by Brookhaven Science Associates, LLC under Contract No. DE-AC02-98CHI-886 with the U.S. Department of Energy. The United States Government retains, and the publisher, by accepting the article for publication, acknowledges, a worldwide license to publish or reproduce the published form of this manuscript, or allow others to do so, for the United States Government purposes.