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 therapy1
. Therefore, one of the greatest challenges in drug addiction treatment is that the individuals who require treatment do not even recognize the need for therapeutic help. This treatment resistance may reflect in part 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 may 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 classical neurological insults (e.g., causing visual neglect or anosognosia for hemiplegia) to classical psychiatric disorders (e.g., schizophrenia, mania and other mood disorders), as recently reviewed2
. 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 network4
. Damage to specific sets of neural circuits may 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 expected4
. An intact interpretive process continues to supply explanations that seem self-evident, even when exceedingly wrong4
(e.g., I am not using my left hand, not because it is paralyzed but because someone is preventing me from using it).
BOX 1: WHAT IS INSIGHT?
The terms insight, interoception, and awareness are often used interchangeably; however, interoception is not synonymous with subjective awareness nor is it clear whether conscious perception of interoceptive signals is sufficient or necessary for insightful action. In general, these terms may be distinguished along the following three lines: (1) sensorimotor
: feeling a particular state, separate from having explicit knowledge of this state; (2) emotional
: might indicate that a person comprehends the implications of a situation, also separate from factual knowledge; and (3) cognitive
: the conscious process of thinking, separate from the recognition or achievement of a goal-state. Importantly, each of these terms has a potentially unique contribution to drug addiction. For example, interoception is defined as the sense of the physiological condition of the entire body or as a generalized homeostatic sensory capacity that underpins a conscious representation of how we feel21
; two of its characteristics are important for addiction. First, interoceptive feelings are associated with intense affective and motivational components. This is not unlike drug cravings, which tend to be linked with overwhelming approach behaviors in heavy users. Second, the motivational evaluation of bodily signals normally depends on the homeostatic state of the individual, as exemplified by the contrasting feelings of reward or punishment produced by a simple cool object at different core body temperatures, yet in addicted individuals such signals may be misinterpreted (e.g., the drug is always wanted as there is no satiety for the drug). Related is the concept that the internal state itself can influence the degree to which individuals are able to accurately report their interoceptive state. For example, individuals with high levels of anhedonia relative to those with no anhedonia were less responsive to emotion-eliciting images across measures of heart rate, affective self-rated mood, and facial expressions69
. In contrast, subjects with high emotional reactivity show high trait anxiety and a high degree of interoceptive awareness based on the heart-beat detection task70, 71
. Similarly, individuals with panic attacks report more cardiac sensations and more frequent aversive interoceptive events than healthy control subjects72
. Parallel studies in addiction are yet to be performed. Finally, one has to consider the correlation between insight/awareness with general intellectual functioning73–76
and study the extent to which cognitive impairment (which has now been reliably documented in drug addiction77, 78
) may increase the risk for impaired self-awareness.
In the current opinion article, we argue that as a cognitive disorder5
, drug addiction may 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) may indicate non-random behavior while the spontaneous attempt to explain this behavior may be compromised or lacking. Specifically, similar to blind-sightedness, where patients report they cannot see the visual cues that actually guide their behavior6
, one could conceptualize drug addiction as a compromised ability to recognize external and internal drug-related
cues. Such attenuated awareness of these cues may 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 may drive these individuals to use drugs excessively, 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 consequences7
. It is also well known that self-reported (conscious) craving is a poor predictor of relapse8
. We recently reported a discordance between self-reported motivation and goal-driven behavior in cocaine addicted individuals9
as illustrated by the forced-choice results depicted in 10
. This discordance is mirrored by brain-behavior dissociations in tasks of reward processing11
, behavioral monitoring and emotional suppression12
. 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 performance14
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).
Figure 1 Self-reported pleasantness ratings (A) and objective choice behavior (total picture viewing selections) on an implicit choice task (B) for each of four picture types (pleasant, unpleasant, neutral, and cocaine) for individuals with cocaine use disorders (more ...)
Although drug addiction may also share with the other neuropsychiatric disorders a resistance to evidence-based or cognitively-driven changes in self-awareness4
, self-awareness enhancements may improve treatment outcome possibly through impact on select neuropsychological functions (e.g., enhancing accuracy of self-report15
, motivation or sense of agency16
). 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 adults17
. In addition, better awareness of severity of alcohol use predicted actual abstinence for up to one year after treatment in 117 male alcoholics18
. Nevertheless, self-awareness enhancements may also increase the salience of negative affect15
, which may lead to increased drug use to alleviate the associated negative affective state. Thus, modulating self-awareness should 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
BOX 2: SELF-AWARENESS AND ALCOHOL
Impairments in social cognition including facial affect perception, emotional prosody, theory of mind, empathy, and related skills (e.g., humor processing) have been documented in alcoholics [review79
]. For example, alcoholics overestimate the intensity of emotions even for neutral faces, with a bias towards overestimation of anger, fear and, in general, negative emotions. This facial affect perception impairment, related to the rostral anterior cingulate cortex and executive dysfunction, may lead to enhanced social conflict, stress and relapse; it may also be ameliorated by abstinence79
. Importantly, these social cognition impairments may be related to self-awareness compromises (e.g., through mechanisms shared by awareness to self and others). In a related conceptualization (reviewed in80, 81
), alcohol reduces the individual's level of self-awareness by inhibiting higher order cognitive processes related to (attending, encoding or sensitivity to) self-relevant information, a sufficient condition to induce and sustain further alcohol consumption. Specifically, this model proposes that alcohol can decrease negative self-evaluation (e.g., self-criticism), providing psychological relief but also decreasing the correspondence between behavior with external and internal standards of appropriate conduct. In support of this model, a series of studies80, 81
showed that (a) alcohol consumption as compared with a placebo control reduced relative usage or recall of self-referenced statements and first-person pronouns (measures of self-evaluation); and (b) high private self-consciousness (a tendency for an individual to direct attention inward towards thoughts, feelings, and behaviors, conceptually similar to interoception) was associated with more
alcohol use (measured by actual drinking in male social drinkers, relapse after three months of detoxification in alcoholics, or self-reported use in adolescents) under negative feedback (failure feedback for performance on a previous task, negative life events, or academic achievement)80, 81
. High private self-consciousness was also associated with higher urge to drink during alcohol cue reactivity paradigms in alcoholics82
. Although moderating factors may include negative mood, reactivity or social context83
, these studies suggest that individuals who are high on interoception or self-awareness may be susceptible to consuming alcohol following personal failure (or other negative reinforcement) where alcohol is used to avoid the ensuing unpleasant self-aware state. These results also suggest that in selected individuals, personal success (or other positive reinforcement) may decrease alcohol (and possibly other drug) consumption. Importantly, these studies suggest that insight manipulations need to take into account the context (e.g., negative or positive) and the baseline propensity of individuals for self-awareness.
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 to neurological patients with focal brain damage19
. 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 attribution5
and neuroadaptations in memory circuits20
, to include compromised interoception, self-awareness and insight into illness.