INTRODUCTION
Attention-deficit/hyperactivity disorder (ADHD) is a childhood-onset disorder, which presents as its main symptoms inattention, hyperactivity and impulsivity. ADHD is the most common childhood psychiatric disorder (8% to 12% of children worldwide), and is also among the most frequent diagnoses deriving from both clinical and neurobiological criteria (Biederman & Faraone, 2005a).
The neurobiological mechanisms underlying ADHD remain relatively unclear. However, there are several bodies of evidence suggesting that ADHD is associated with structural and functional abnormalities in fronto-subcortical neural circuitry, including regions such as the cerebellum and the corpus callosum (Biederman & Faraone 2005b). Decreased functional activity of the dopaminergic and noradrenergic systems has also been implicated in the pathogenesis of ADHD (Biederman & Faraone, 2005b).
Although during childhood and adolescence the prevalence of ADHD among males is higher than that among females, the overall prevalence of ADHD in adulthood is about 3% to 5%, whereas the differential between adult males and females no longer appears significant (Biederman & Faraone, 2005a). Despites its relatively high prevalence, ADHD in adults is far less studied, and consequently far less understood. The idea that ADHD can persist in adults has been a matter of debate for several decades, and nowadays, adulthood diagnosis of ADHD is often neglected (McGough & Barkley, 2004). We now have a large body of evidence showing that at least half of the children with the disorder continue to show signs of impairment in adulthood, and, as a consequence, these patients frequently exhibit abnormal behaviors, such as antisocial behaviors, problems with peers, poor occupational performance, traffic violations, and vehicle accidents (Biederman & Faraone, 2005b).
Neuropsychological deficits are frequently described in adults with ADHD in domains such as memory, attention, and executive functions (Hervey et al., 2004). It is a well-known fact that the key symptoms of this disorder are associated with poor performance in many aspects of executive functions (Willcutt et al., 2005). Despite this strong evidence, which is confirmed in children, there is considerable debate over whether such neuropsychological impairments are evident in adults with ADHD (Nigg et al., 2005; Willcutt et al., 2005).
According to Barkley (1997), the ability to inhibit responses is a core deficit in ADHD, which then lead to executive dysfunction. Several studies support this notion of inhibitory control deficit in adults with ADHD, using behavioral paradigms of motor response inhibition, such as the Continuous Performance Task (CPT). Indeed, adults with ADHD tend to commit more commission errors on the CPT than controls (Hervey et al., 2004).
Some authors hold that the symptoms of hyperactivity and impulsivity, as opposed to inattention, tend to decrease at a higher rate in adolescence and early adulthood (Biederman et al., 2000). Nonetheless, some studies have shown that impulsivity persists in adults with ADHD (Epstein et al., 2003), and have also suggested that this symptom might be the underlying mechanism of many of the behavioral dysfunctions seen in adults with ADHD (Babinski et al., 1999).
Impulsiveness can be defined as a process that includes a swift action without conscious judgment, a behavior without adequate thought, and a tendency to act with less forethought, despite displaying normal intelligence (Moeller et al., 2001). Several authors have divided the construct of impulsiveness into several different dimensions. For instance, Barratt (Patton et al., 1995) maintains that impulsive behavior comprises three components: motor (action without thinking), attentional (lack of focus on the task at hand), and non-planning (orientation towards the present, rather than to the future). This classification presents some convergence on Bechara's model (Bechara et al., 2000a), who argues that there is a functional and structural difference between motor impulsivity, which is related to inhibition of pre-potent responses, and decision-making which in one instance was also referred to as “cognitive impulsivity.” This type of impulsivity seems analogous to Barratt's non-planning impulsivity. According to Bechara's model, motor and cognitive impulsivity also depend on separate neural regions: the former is related to the more posterior regions of the orbitofrontal/ventromedial prefrontal cortex, including the basal forebrain, and the latter is related to the more anterior orbitofrontal/ventromedial prefrontal cortex, including the frontal pole. Bechara also discusses another cognitive type of impulsivity, concerning working memory and the ability to inhibit irrelevant information held in working memory and to focus on the task at hand. This type of impulsivity is linked to the dorsolateral prefrontal cortex, and may be analogous to the attentional impulsivity aspect described by Barratt. It is important to note, however, that neurally speaking, attentional and motor impulsivity may not be easily separable under normal circumstances, because any neuropsychological task that involves inhibition of a motor response (a downstream process), may also invoke an “upstream” process of attending and intending to inhibit the response in question.
Traditional measures of impulsive behaviors in individuals with ADHD have included the “Stroop Color Word,” “CPT,” “Wisconsin Card Sorting Test,” “Stop Signal Reaction Time.” These tasks are likely to engage and measure the motor and attentional facets of impulsivity. Only a small number of studies have addressed decision-making or cognitive impulsivity in ADHD and this is especially true in the case of adult ADHD. Most of these studies have used the Iowa Gambling Task (IGT) (Bechara et al., 2000b), a paradigm that is believed to model real-life decision-making, especially the type of decisions that are consistent with the construct of “cognitive impulsiveness.” Using an adaptation of IGT for children, Garon et al. (2006) found deficits in decision-making in children with pure ADHD (n = 11), compared to children with ADHD associated with internalizing symptoms (n = 11), and to matching controls (n = 21). Using the IGT, Toplak et al., (2005) showed a pattern of poor decision-making in adolescents with ADHD (n = 36), in comparison to controls (n = 34). These results were similar to those reported by Ernst et al., (2003a) in a study comparing adolescents with disruptive behaviors (including ADHD) with matching controls.
In a study of the neural basis of decision-making in adults with ADHD, Ernst et al., (2003b) found no differences among ADHD adults (n = 10) and healthy controls (n = 12) in terms of their net scores on the IGT. However, the brain activation measured by positron emission tomography (PET) revealed differences between the two groups. Adults with ADHD showed increased activity in the caudal part of the right cingulate cortex relative to controls, and relatively weaker activity in the hippocampus and insular cortex. This finding suggests that there are differences between adults with ADHD and comparison controls in the way they engage specific functional neural circuits during the pondering and execution of behavioral decisions. Perhaps this difference may explain the problems presented by ADHD subjects in everyday life.
The main objective of our study was to address the issue of impulsivity in adult ADHD, and examine whether the three facets of impulsivity: attentional, non-planning, and motor impulsivity are present. Most importantly, we sought to address how these self-report measures of impulsivity may relate to parallel neuropsychological models of impulse control. We studied a well-characterized sample of adults with ADHD using self-report measures of impulsivity, and using neuropsychological tasks believed to tax different mechanisms of impulse control.
METHODS
Participants
We assessed 50 adults with ADHD (22 women and 28 men) recruited from the research group on learning disabilities, attention, and hyperactivity (GEDAHI), and 51 comparison (control) subjects (31 women and 20 men) recruited through local advertisements. An ADHD diagnosis was assigned to an individual after meeting the DSM-IV criteria for ADHD, and additionally after a consensus was reached on two independent interviews conducted separately, by a neurologist and a psychologist. Furthermore, as another inclusion criterion for the study, participants had to have scores greater than or equal to the 25th percentile on the Raven progressive matrices, an educational level above eight years of formal education, and an age between 18 and 60 years.
We excluded participants with a current major depressive disorder or manic/hippomanic episode, substance-related disorders, psychotic disorders, obsessive-compulsive disorder, or a lifetime history of traumatic brain Injury/vascular brain disorder. To assess psychiatric symptoms among study subjects, we used the Mini-Neuropsychiatric Interview (MINI 5.0; Sheehan et al.,1998).
In the ADHD group, according to DSM-IV classification criteria of ADHD, we had 14 subjects of the “inattentive” type, and 36 subjects of the “combined” type. There were none of the “hyperactive/impulsive” type. Among these subjects, we found 14 with past history of depressive symptoms, and 5 with past history of drug use. We also found 14 subjects who met the criteria for generalized anxiety disorder.
On the day of the neuropsychological assessment, none of the ADHD individuals had used methylphenidate or any other medication used in the treatment of symptoms of inattention and/or hyperactivity. None of the patients was using long-lasting methylphenidate.
Instruments
The Barratt impulsivity scale Version 11 (BIS, Patton et al., 1995), a 30-item, self-report questionnaire, was used in this study. This instrument has 3 sub-scales: non-planning impulsivity (orientation towards the present rather than to the future), motor impulsivity (fast reactions and restlessness), and attentional impulsivity (problems related to concentrating/paying attention).
The CPT-II (Epstein et al., 2003) provides measures of sustained attention and impulsiveness. On this task, the subject has to press a spacebar when any letter (except for the letter X) appears on screen. An omission error occurs when the subject fails to press the spacebar when a letter (except for X) appears, thus reflecting an instance of failure of the subject react to the target stimulus. A commission error occurs when the subject presses the spacebar when an X letter appears on the screen, thus reflecting a failure to inhibit a pre-potent motor response. We considered these two measures as corresponding to the concepts of attentional and motor impulsiveness, respectively, in Barratt's model of impulsiveness. Therefore we used omission and commission errors as dependent measures to evaluate attentional and motor impulsivity, respectively.
Subjects completed the computerized version of the IGT (Bechara et al.,2000b). Details of this procedure are described elsewhere (Bechara et al., 2000b). Briefly, subjects have to choose one card at a time from 4 available decks (A, B, C, and D). The task requires subjects to make 100 choices (100 trials), and in each trial, subjects may win or lose a certain amount of money. Two of the decks yield relatively high immediate gain, but in the long run they incur higher loss, and thus are disadvantageous. In contrast, the other decks yield relatively lower gains, but in the long run they incur smaller losses, and thus are advantageous. Over the trials, normal subjects learn to avoid the disadvantageous decks in preference for the advantageous ones. To measure performance, choices are divided into five blocks, with 20 choices each. For each block, a net score [number of cards selected from the advantageous (good) decks minus the disadvantageous (bad) decks] is obtained. A total net score from all blocks is also obtained. The blocks as well as the total net scores were used as dependent measures.
Procedures
A trained neuropsychologist (L.M-D.) administered the tests in a laboratory, and in a fixed order: CPTII-IGT-BIS-11. The examiner was blind to the diagnosis of the subject being tested. The Local Ethics Review Committee had approved the study protocol. All participants signed informed consents before participating in this study.
Analyses
Our analyses consisted of one-way ANOVAs, as well as Pearson Coefficient analyses for correlations between measures obtained from the ADHD group. We have also used the Pearson χ2 to test differences in dichotomous measures, such as gender distribution among the groups.
RESULTS
Differences between the two groups concerning gender, age, education, and intelligence, as measured by the Raven Progressive Matrices, were not significant (Table 1).
Comparison between sociodemographic characteristics and test performance of comparison (control) and ADHD groups
We found significant differences between ADHD and comparison (control) subjects on several measures (Table 1). Briefly, on the BIS, we found a significant difference between the two groups in the total score, as well as the attentional, motor, and non-planning impulsivity scores. On the CPT-II, the ADHD group committed significantly more errors of omission and commission, relative to the comparison (control) group. On the IGT, we found significant differences between the two groups in the third, fourth, and fifth block. In these three blocks, ADHD individuals had significantly lower net scores than control individuals (Fig. 1). The total net score from the IGT was also significantly smaller in the ADHD group, versus the comparison (control) group.
Number of cards selected from the advantageous (CD) minus disadvantageous decks (AB) on the Iowa Gambling Task (IGT), which were obtained from the comparison (controls) and patient's in Igt's difference between advantageous and disadvantageous choices groups. Net scores (CD minus AB) are presented as means ± SEM across five blocks of cards (20 cards each).
In the ADHD Group, we found a positive correlation between omission errors on the CPT-II, and the attentional score of the BIS (r = .461). We did not find any significant correlation between BIS's motor impulsivity scores and commission errors from the CPT-II (r = 1.48).The non-planning scores of the BIS were negatively correlated with the net scores of the IGT in the second (r = −0.376), third (r = −.397), fourth (r = −.464), and fifth (r = .387) blocks. We also found a negative correlation between the total net score of the IGT and the non-planning score of the BIS (r = −.572). The total score of BIS presented a negative correlation with the difference between advantageous and disadvantageous choices in the second block (r = −.313), third block (r = −.31) and net IGT score (r = −.319).
DISCUSSION
Our data provides support for the hypothesis that deficits exist related to three components of impulsivity: motor, cognitive, and attentional, in adults with ADHD. The ADHD group did not differ from controls on scores for general intelligence, which indicate that the deficits evidenced in measures of impulsiveness are not explained by differences in cognitive measures, such as general intelligence. These results are consistent with Barkley's hypothesis of inhibitory deficit in adults with ADHD (Barkley, 1997). Most notably, our results reveal the importance of going beyond the use of self-report measures of motor and attentional impulsivity in order to gain a better understanding of the neurobiology of ADHD and its symptomatology.
Several studies have shown evidence for motor impulsivity in children and adults with ADHD (Hervey et al., 2004). In our study, although we did not find significant correlations between BIS motor impulsivity scores and commission errors from the CPT-II, both sets of measures scored nonetheless worse in the ADHD group, relative to controls. This suggests that adults with ADHD exhibit impairments in a specific neural mechanism of impulse control, such as that detected by the CPT-II. This data is in accordance with Barkley's theory (1997), which suggests that ADHD subjects show behavioral impairments when they need to inhibit a pre-potent motoric response. According to Barkley (1997), this is a core deficit presented by children and adults with ADHD, although several investigators have argued that this deficit is insufficient to explain all of the neurocognitive deficits in this population (Hervey et al., 2004). It has been proposed that a neural circuitry involving the dorsolateral prefrontal cortex and the most posterior aspect of the ventromedial prefrontal cortex (i.e., the anterior cingulate cortex and basal forebrain), and modulated by the dopaminergic fronto-striatal system, may be implicated in this type of impulse control (Bechara & Van der Linden, 2005).
Cognitive impulsivity, on the other hand, has tended to be linked to the orbitofrontal/ventromedial areas of the prefrontal cortex, especially the more anterior sector of this region—the frontal pole (Bechara et al., 2000a). This function may also be more sensitive to the modulation of the serotonergic system (Rogers et al., 2003). Whether an orbitalfrontal/ventromedial prefrontal dysfunction underlies some of the behavioral manifestations in ADHD remains unclear, but some evidence has suggested that this prefrontal region may be involved in the pathogenesis of the disorder. In our study, the ADHD group showed poorer performance on the IGT than healthy volunteers. Specifically, we observed that the ADHD group made significantly more disadvantageous choices than controls, especially in the last three blocks of trials on the IGT. These findings are consistent with previous studies reporting that individuals with ADHD make more disadvantageous choices on this task relative to controls (Garon et al., 2006; Toplak et al., 2005).
In the ADHD group, the negative correlation between the net scores in the second, third, fourth, and fifth blocks of the IGT, and the non-planning scores of the BIS supports the hypothesis that cognitive impulsivity is present in adults with ADHD. Furthermore, these results also suggest that the constructs of Barratt's non-planning impulsivity and Bechara's decision-making or cognitive impulsivity might be related. Indeed, it has been previously suggested that these two personality and neuropsychology constructs of impulsivity could be related. However, no empirical evidence in support of such a relationship has yet been presented. The current results do provide such evidential support. Furthermore, the current results corroborate findings (Zermatten et al., 2005) suggesting that another construct of impulsivity, “premeditation” (Whiteside & Lynam, 2001), which seems analogous to Barratt's non-planning impulsivity (e.g., see Bechara & Van der Linden, 2005), is also related to decision-making, as measured by the IGT.
Akin to other authors (Toplak et al., 2005), we did not find correlations between measures of executive functions (CPT-II's commission and omission errors) and performance on the IGT. These results further support the notion that these two facets of impulsive behaviors might be separate.
Epstein et al. (2003) did not find a relationship between symptoms of inattention, according DSM-IV criteria and omission errors on the CPT-II, although ADHD subjects made more errors than normal controls. In our study we also found that the ADHD group made more omission errors than control subjects. These data are in accordance with studies that showed a persistence of attentional deficits in adults with ADHD (Nigg et al., 2005). Additionally, we found a relationship between attention score of the BIS and omission errors on the CPT-II. This correlation points to the importance of attention impulsivity in explaining the omission errors in CPT-II.
The clinical and cross-sectional nature of the present study somewhat compromises the generalization of the current results. Additional limitations of the current study, similar to previous neuropsychological studies of ADHD (Hervey et al., 2004), include the relatively small sample size, in comparison with an epidemiological sample for instance. The small sample size limits the ability to make proper comparisons between inattentive and combined subtypes of ADHD, or between ADHD subgroups with different co-morbid disorders. The effects of different ADHD subtypes and comorbid conditions on the three different facets of impulsiveness addressed in the current study should be investigated in future studies.
In conclusion, this study emphasizes the importance of using complementary approaches in the study of impulsivity, where our results are consistent with a previous study suggesting that impulsivity is a multi-dimensional construct, which should be investigated through the use of different methods and approaches (Fuentes et al., 2006). Further studies should explore possible relationships between various performance measures on neuropsychological tasks and a range of ADHD variables, such as symptom severity.
ACKNOWLEDGMENT
This work was supported by the Learning, Attention, and Hyperactivity Disorders Research Group (GEDAHI).
