Response inhibition and impulsivity: an fMRI study
Introduction
Impulsivity is a multidimensional concept that incorporates failure of response inhibition, rapid processing of information, novelty seeking, and inability to delay gratification (Barratt, 1985, Barratt, 1994). Impulsivity is one of the defining characteristics of a number of psychiatric diagnoses, particularly borderline and antisocial personality disorders (Stein et al., 1993, Stein et al., 1995). Poor impulse control correlates significantly with suicidal, violent and aggressive behaviour (Plutchik and Van Praag, 1989, Plutchik and Van Praag, 1995) and is an increasingly important aspect of risk assessment in a variety of clinical situations, including assessment of dangerousness (Monahan et al., 2000). Most attempts to measure impulsivity rely on psychometric self-report trait measures. Some behavioural impulsivity tasks have been developed, measuring preference for a smaller more immediate reward over a delayed larger reward, and impaired motor inhibition, however, psychometric and behavioural impulsivity measures do not correlate well with each other (Barratt and Patton, 1983, Barratt et al., 1997). Behavioural impulsivity tasks tend to have low test–retest reliability, apart from the Go/NoGo task, which has reasonable temporal stability (Kindlon, Mezzacappa, & Earls, 1995).
Impulsivity is a feature of damage to the frontal lobe and an “acquired sociopathic” syndrome has been described following ventromedial frontal lobe lesions (Damasio, Tranel, & Damasio, 1990; Grafman et al., 1996; Paradiso et al., 1999, Paradiso et al., 1999). This has lead to suggestions that impaired ventromedial frontal lobe function may contribute to poor impulse control in antisocial personality disorders (Damasio, 2000). In support of this notion a variety of neuropsychological deficits have been reported in antisocial populations (Morgan & Lilienfeld, 2000). Neuroimaging studies in this population report a reduction in prefrontal metabolism (Raine, Buchsbaum, & LaCasse, 1997), and reduced prefrontal grey matter volumes (Raine, Lencz, Bihrle, La Casse, & Colletti, 2000).
Positron emission tomography (PET) (Kawashima et al., 1996; Krams et al., 1998, Nobre et al., 1999) and functional Magnetic Resonance Imaging (fMRI) studies (Casey et al., 1997; Garavan, Ross, & Stein, 1999; Hager et al., 1998; Konishi, Nakajima, Uchida, Sekihara, & Miyashita, 1998) of response inhibition and processing novel stimuli suggest a role for the prefrontal cortex, especially the right lateral frontal cortex, and a network of associated regions in response inhibition. It is not clear to what extent these inhibition-related activations may depend on subjects’ impulsivity. Garavan, Ross, Murphy, Roche, & Stein (2002) have reported greater reliance on anterior cingulate cortex during Go/NoGo in subjects who are more absent-minded, using a cognitive measure that they have found to be correlated with Barrett’s Impulsivity Scale (BIS). The key novel aspect of the present study is the direct investigation of the relationship between trait impulsivity measures and blood oxygen level dependent (BOLD) response.
We hypothesized that: (1) orbitofrontal cortex would be activated during response inhibition, (2) low scores on psychometric (trait) impulsivity measures would be associated with greater activation in orbitofrontal cortex during response inhibition, (3) low error-rates on the Go/NoGo response inhibition task would be associated with greater activation in the orbitofrontal cortex during response inhibition, (4) psychometric (trait) impulsivity scores would correlate positively with error-rate on response inhibition tasks.
Section snippets
Subjects
Twenty-one subjects were recruited by advertisement at their work-places. All subjects were male, right-handed, aged 18–50 years, and employed by the National Health Service or the University of Manchester. The Local Research Ethics Committee granted ethical approval. Subjects participated in a Structured Clinical Interview (SCID-NP) (Spitzer, Williams, Gibbon, & First, 1990) administered by a psychiatrist. Exclusion criteria were: current DSM III-R psychiatric axis I disorder, neurological
Results
Of 21 subjects recruited, 1 subject withdrew from the study, and 20 subjects completed the psychometric and behavioural impulsivity assessments. Although subjects were not explicitly informed of their performance during the Go/NoGo task it was observed the training session that subjects knew immediately when they had made errors. One further subject did not attend the scanning session, so we analysed complete imaging data for 19 subjects. One subject’s performance data in the scanned Go/NoGo
Psychometric (trait) and behavioural measures of impulsivity
We found no correlations between trait impulsivity measures and errors of commission on the Go/NoGo task. Instead we found that lower IQ was strongly associated with more errors of commission in both the correlation and the factor analysis (see factor 2 Table 4). This suggests that intelligence rather than impulsivity may be the main source of variation in a simple Go/NoGo task.
Brain activation during response inhibition
The most significant neural responses during the NoGo condition were seen in right anterior lateral anterior
Conclusions
Our findings support the hypothesis that the anterior lateral orbitofrontal cortex is activated during response inhibition. In addition, a network of higher order association and paralimbic areas was activated. While these regions are known to be anatomically connected and have been activated in this study, the challenge of elucidating the precise sequences of neural activity will require more sophisticated techniques, such as the use of brain evoked-potential measurement and event-related fMRI
Acknowledgements
This study was supported with funding from the Mental Health Services of Salford and the Wellcome Trust. The authors thank the staff of the Neuroimaging Analysis Centre, University of Manchester for assistance, particularly: Dr. I. Holländer, Lecturer in functional MRI, Department of Gastroenterology and Ms. Y. Watson, Superintendent Radiographer, Department of Clinical Radiology.
References (38)
- et al.
Neuropsychological and cognitive psychophysiological substrates of impulsive aggression
Biological Psychiatry
(1997) - et al.
Individuals with psychopathic behaviour caused by frontal damage fail to respond autonomically to social stimuli
Brain and Behaviour Research
(1990) - et al.
Dissociable executive functions in the dynamic control of behaviour: Inhibition, error detection and correction
Neuroimage
(2002) - et al.
Functional anatomy of GO/NO-GO discrimination and response selection—A PET study in man
Brain Research
(1996) - et al.
Brain abnormalities in murderers indicated by positron emission tomography
Biological Psychiatry
(1997) - Barratt, E. S. (1985). Impulsiveness defined within a systems model of personality. In E. P. Speilburger, & J. N....
- Barratt, E. S. (1994). Impulsiveness and aggression. In J. Monahan, & H. Steadman (Eds.), Violence and mental disorder:...
- Barratt, E. S., & Patton, J. H. (1983). Impulsivity: Cognitive, behavioral, and psychophysiological correlates. In M....
- et al.
A developmental functional MRI study of prefrontal activation during performance of a Go-No-Go task
Journal of Cognitive Neuroscience
(1997) A neural basis for sociopathy
Archives of General Psychiatry
(2000)
Relatinship between 5-HT function and impulsivity and aggression in male offenders with personality disorders
British Journal of Psychiatry
Dissociable functions in the medial and lateral orbitofrontal cortex: Evidence from human neuroimaging studies
Cerebral Cortex
Statistical parametric maps in functional imaging: A general approach
Human Brain Mapping
Right hemispheric dominance of inhibitory control: An event-related functional MRI study
Proceedings of the National Academy of Sciences USA
Brain activity during transient sadness and happiness in healthy women
American Journal of Psychiatry
Frontal lobe injuries, violence, and aggression: A report of the Vietnam Head Injury Study
Neurology
Challenging the anterior attentional system with a continuous performance task: A functional magnetic resonance imaging approach
European Archives of Psychiatry and Clinical Neuroscience
Statistical modelling of low-frequency compounds in fMRI
Neuroimage
Cited by (489)
Impulsivity and neural correlates of response inhibition in bipolar disorder and their unaffected relatives: A MEG study
2024, Journal of Affective DisordersImpaired inhibition after delta-9-tetrahydrocannabinol in women not related to circulating estradiol levels
2023, Pharmacology Biochemistry and BehaviorA framework for understanding reasoning errors: From fake news to climate change and beyond
2023, Advances in Experimental Social Psychology