Decreased saliency processing as a neural measure of Barratt impulsivity in healthy adults

Cognitive control is necessary to navigating through an uncertain world. With the stop signal task (SST), we measure how cognitive control functions in a controlled environment. There has been conflicting evidence on whether trait impulsivity might reflect differences in cognitive control during the SST. While some studies find that trait impulsivity relates to measures of response inhibition, such as the stop signal reaction time (SSRT), other studies do not. Here, in 92 young adult participants (58 females; age 25 ± 4 years), we examined whether trait impulsivity, measured by the Barratt impulsivity scale (BIS-11), is associated with differences in performance and regional brain activations for the component processes of cognitive control during the SST. Across participants, trait impulsivity showed a trend-level correlation with SSRT (F(1.90)=3.18, p<.07; Pearson regression). In simple regressions, activation of the right anterior dorsal insula and middle frontal cortex (MFC) during stop as compared to go trials negatively correlated with motor and non-planning impulsivity score. Using the generalized form of psychophysiological interaction (gPPI), we showed that functional connectivity of the right insula and MFC with the left dorsolateral prefrontal cortex and bilateral visual areas were also negatively correlated with impulsivity. None of the other component processes of cognitive control, including response inhibition, error processing, post-error slowing, were significantly related to Barratt impulsivity. These results suggest that trait impulsivity as measured by BIS-11 may have distinct effects on saliency processing in adult individuals.

[1]  Christoph Stahl,et al.  Impulsivity in Borderline Personality Disorder: Impairment in Self-Report Measures, but Not Behavioral Inhibition , 2010, Psychopathology.

[2]  Jan Theeuwes,et al.  Endogenous and exogenous attention shifts are mediated by the same large-scale neural network , 2004, NeuroImage.

[3]  Shenmin Zhang,et al.  Saliency Processing and Obesity: A Preliminary Imaging Study of the Stop Signal Task , 2012, Obesity.

[4]  M. Hallett,et al.  Aberrant supplementary motor complex and limbic activity during motor preparation in motor conversion disorder , 2011, Movement disorders : official journal of the Movement Disorder Society.

[5]  Katya Rubia,et al.  Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection , 2003, NeuroImage.

[6]  Carrie L. Masten,et al.  Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation. , 2013, Social cognitive and affective neuroscience.

[7]  K. R. Ridderinkhof,et al.  Probability effects in the stop-signal paradigm: The insula and the significance of failed inhibition , 2006, Brain Research.

[8]  Sheng Zhang,et al.  Functional connectivity mapping of the human precuneus by resting state fMRI , 2012, NeuroImage.

[9]  Katya Rubia,et al.  An fMRI study of reduced left prefrontal activation in schizophrenia during normal inhibitory function , 2001, Schizophrenia Research.

[10]  Sheng Zhang,et al.  Functional networks for cognitive control in a stop signal task: Independent component analysis , 2012, Human brain mapping.

[11]  Samuel M. McClure,et al.  Social Anxiety Modulates Risk Sensitivity through Activity in the Anterior Insula , 2012, Front. Neurosci..

[12]  N. Farb,et al.  Attentional modulation of primary interoceptive and exteroceptive cortices. , 2013, Cerebral cortex.

[13]  Amit Etkin,et al.  Functional neuroanatomy of anxiety: a neural circuit perspective. , 2010, Current topics in behavioral neurosciences.

[14]  Luis Carretié,et al.  Automatic attention to emotional stimuli: Neural correlates , 2004, Human brain mapping.

[15]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[16]  M. Mesulam,et al.  The central role of the prefrontal cortex in directing attention to novel events. , 2000, Brain : a journal of neurology.

[17]  C. Li,et al.  Behavioral/systems/cognitive Functional Connectivity Delineates Distinct Roles of the Inferior Frontal Cortex and Presupplementary Motor Area in Stop Signal Inhibition , 2022 .

[18]  W. Penny,et al.  Random-Effects Analysis , 2002 .

[19]  E. Barratt,et al.  Psychiatric aspects of impulsivity. , 2001, The American journal of psychiatry.

[20]  W. D. Penny,et al.  Random-Effects Analysis , 2002 .

[21]  Adam R Aron,et al.  Methylphenidate improves response inhibition in adults with attention-deficit/hyperactivity disorder , 2003, Biological Psychiatry.

[22]  Monica Luciana,et al.  Reward-related decision-making deficits and elevated impulsivity among MDMA and other drug users. , 2008, Drug and alcohol dependence.

[23]  C. Rorden,et al.  Cognitive Control Mechanisms Revealed by ERP and fMRI: Evidence from Repeated Task-Switching , 2003, Journal of Cognitive Neuroscience.

[24]  Jin Fan,et al.  Cognition-emotion integration in the anterior insular cortex. , 2013, Cerebral cortex.

[25]  J. Downar,et al.  A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. , 2002, Journal of neurophysiology.

[26]  Sue-Huei Chen,et al.  Attentional blink in adolescents with varying levels of impulsivity. , 2005, Journal of psychiatric research.

[27]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[28]  Donald R. Lynam,et al.  Understanding the role of impulsivity and externalizing psychopathology in alcohol abuse: Application of the UPPS Impulsive Behavior Scale. , 2009 .

[29]  Christoph Mulert,et al.  Neuroimaging in anxiety disorders , 2011, Dialogues in clinical neuroscience.

[30]  T. Robbins,et al.  Behavioral models of impulsivity in relation to ADHD: Translation between clinical and preclinical studies , 2006, Clinical psychology review.

[31]  John J. Foxe,et al.  Predicting Success: Patterns of Cortical Activation and Deactivation Prior to Response Inhibition , 2004, Journal of Cognitive Neuroscience.

[32]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[33]  Keiji Tanaka,et al.  Mnemonic Function of the Dorsolateral Prefrontal Cortex in Conflict-Induced Behavioral Adjustment , 2007, Science.

[34]  Brian Knutson,et al.  Ventral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics , 2009, Biological Psychiatry.

[35]  Rinus G. Verdonschot,et al.  Neural mechanisms underlying the induction and relief of perceptual curiosity , 2012, Front. Behav. Neurosci..

[36]  R T Knight,et al.  Anatomic bases of event-related potentials and their relationship to novelty detection in humans. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[37]  G. Logan,et al.  On the ability to inhibit simple and choice reaction time responses: a model and a method. , 1984, Journal of experimental psychology. Human perception and performance.

[38]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  M. Carrillo-de-la-Peña,et al.  Comparison among Various Methods of Assessment of Impulsiveness , 1993, Perceptual and motor skills.

[40]  Rajita Sinha,et al.  Neural Correlates of Impulse Control During Stop Signal Inhibition in Cocaine-Dependent Men , 2008, Neuropsychopharmacology.

[41]  César Ávila,et al.  Personality and inhibitory deficits in the stop-signal task: the mediating role of Gray’s anxiety and impulsivity , 2001 .

[42]  Heather A. Wilk,et al.  Brain regions associated with moment-to-moment adjustments in control and stable task-set maintenance , 2012, NeuroImage.

[43]  Ian M. Anderson,et al.  Neural correlates of choice behavior related to impulsivity and venturesomeness , 2011, Neuropsychologia.

[44]  M. Preul The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy , 2001 .

[45]  Y. Okamoto,et al.  Negative correlation between right prefrontal activity during response inhibition and impulsiveness: A fMRI study , 2004, European Archives of Psychiatry and Clinical Neuroscience.

[46]  M. Miyazaki,et al.  The role of the dorsolateral prefrontal cortex in the inhibition of stereotyped responses , 2010, Experimental Brain Research.

[47]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[48]  Kent E Hutchison,et al.  Neural mechanisms of risk taking and relationships with hazardous drinking. , 2012, Alcoholism, clinical and experimental research.

[49]  Jaime S. Ide,et al.  Human Neuroscience , 2022 .

[50]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.

[51]  X. Hu,et al.  4 T-fMRI study of nonspatial shifting of selective attention: cerebellar and parietal contributions. , 1998, Journal of neurophysiology.

[52]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[53]  E. Crone,et al.  Neural evidence for dissociable components of task-switching. , 2006, Cerebral cortex.

[54]  J. Patton,et al.  Factor structure of the Barratt impulsiveness scale. , 1995, Journal of clinical psychology.

[55]  L. Schreiber,et al.  A neurocognitive comparison of cognitive flexibility and response inhibition in gamblers with varying degrees of clinical severity , 2011, Psychological Medicine.

[56]  Chiang-shan Ray Li,et al.  Neural correlates of speeded as compared with delayed responses in a stop signal task: an indirect analog of risk taking and association with an anxiety trait. , 2009, Cerebral cortex.

[57]  J. Anton,et al.  Impulsivity and neural correlates of response inhibition in schizophrenia , 2010, Psychological Medicine.

[58]  Antoni Rodríguez-Fornells,et al.  Are high-impulsive and high risk-taking people more motor disinhibited in the presence of incentive? , 2002 .

[59]  M. Spinella NORMATIVE DATA AND A SHORT FORM OF THE BARRATT IMPULSIVENESS SCALE , 2007, The International journal of neuroscience.

[60]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[61]  H. Duvernoy,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy with MRI, and Blood Supply , 1999 .

[62]  Charles W. Mathias,et al.  Comparisons of women with high and low trait impulsivity using behavioral models of response-disinhibition and reward-choice , 2002 .

[63]  David Badre,et al.  Analogical reasoning and prefrontal cortex: evidence for separable retrieval and integration mechanisms. , 2004, Cerebral cortex.

[64]  Sien Hu,et al.  The effects of age on cerebral activations: internally versus externally driven processes , 2012, Front. Ag. Neurosci..

[65]  N Kathmann,et al.  Impaired decision making and feedback evaluation in borderline personality disorder , 2011, Psychological Medicine.

[66]  Jaime S. Ide,et al.  A cerebellar thalamic cortical circuit for error-related cognitive control , 2011, NeuroImage.

[67]  C. Frith,et al.  Neural correlates of change detection and change blindness , 2001, Nature Neuroscience.

[68]  H. Garavan,et al.  Dissociable Executive Functions in the Dynamic Control of Behavior: Inhibition, Error Detection, and Correction , 2002, NeuroImage.

[69]  A. T. Smith,et al.  Attentional suppression of activity in the human visual cortex , 2000, Neuroreport.

[70]  J L Kenemans,et al.  Differences between low and high trait impulsivity are not associated with differences in inhibitory motor control , 2004, Journal of attention disorders.

[71]  Deborah A. Day,et al.  Information processing in the child: Significance of analytic and reflective attitudes. , 1964 .

[72]  G. Logan On the ability to inhibit thought and action , 1984 .

[73]  S. Woods,et al.  Will the novel antipsychotics significantly ameliorate neuropsychological deficits and improve adaptive functioning in schizophrenia? , 1999, Psychological Medicine.

[74]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[75]  M. Angstadt,et al.  Insula reactivity and connectivity to anterior cingulate cortex when processing threat in generalized social anxiety disorder , 2012, Biological Psychology.

[76]  R. T. Constable,et al.  Error-specific medial cortical and subcortical activity during the stop signal task: A functional magnetic resonance imaging study , 2008, Neuroscience.

[77]  G. Logan,et al.  In search of the point of no return: the control of response processes. , 1990, Journal of experimental psychology. Human perception and performance.

[78]  C. Li,et al.  Neural processes of preparatory control for stop signal inhibition , 2012, Human brain mapping.

[79]  M Corbetta,et al.  Multiple neural correlates of detection in the human brain. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[80]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[81]  T. Hanakawa,et al.  Transient Neural Activity in the Medial Superior Frontal Gyrus and Precuneus Time Locked with Attention Shift between Object Features , 1999, NeuroImage.

[82]  T. Robbins,et al.  Review Personality, Addiction, Dopamine: Insights from Parkinson's Disease Table 1. Possible Site of Striatal Dopamine Dysfunction Causing Different Motor and Cognitive Symptoms in Parkinson's Disease , 2022 .

[83]  Mario Liotti,et al.  Inhibitory control in children with attention-deficit/hyperactivity disorder: event-related potentials identify the processing component and timing of an impaired right-frontal response-inhibition mechanism , 2000, Biological Psychiatry.

[84]  Gian Luca Romani,et al.  Somato-motor inhibitory processing in humans: An event-related functional MRI study , 2008, NeuroImage.

[85]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[86]  Marta I. Garrido,et al.  Functional Evidence for a Dual Route to Amygdala , 2012, Current Biology.

[87]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[88]  W. van den Brink,et al.  The role of self-reported impulsivity and reward sensitivity versus neurocognitive measures of disinhibition and decision-making in the prediction of relapse in pathological gamblers , 2007, Psychological Medicine.

[89]  Luiz Pessoa,et al.  Impact of state anxiety on the interaction between threat monitoring and cognition , 2012, NeuroImage.

[90]  Jim M. Monti,et al.  Neural Integration of Top-Down Spatial and Feature-Based Information in Visual Search , 2008, The Journal of Neuroscience.

[91]  I. Robertson,et al.  The Role of a Right Fronto-Parietal Network in Cognitive Control: Common Activations for Cues-to-Att , 2006 .

[92]  Hiroshi Fukuda,et al.  Functional anatomy of GO/NO-GO discrimination and response selection — a PET study in man , 1996, Brain Research.

[93]  Y. Miyashita,et al.  Preparation to Inhibit a Response Complements Response Inhibition during Performance of a Stop-Signal Task , 2009, The Journal of Neuroscience.

[94]  A. Rangel,et al.  Dissociating valuation and saliency signals during decision-making. , 2011, Cerebral cortex.

[95]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[96]  J Kagan,et al.  Conceptual impulsivity and inductive reasoning. , 1966, Child development.

[97]  Louis A. Schmidt,et al.  Social fearfulness in the human brain , 2012, Neuroscience & Biobehavioral Reviews.

[98]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[99]  C. Li,et al.  Dissociable Processes of Cognitive Control during Error and Non-Error Conflicts: A Study of the Stop Signal Task , 2010, PloS one.

[100]  L. Clark,et al.  Impulsivity and cognitive distortions in pathological gamblers attending the UK National Problem Gambling Clinic: a preliminary report , 2011, Psychological Medicine.

[101]  M. Hughes,et al.  The spatial and temporal dynamics of anticipatory preparation and response inhibition in task-switching , 2010, NeuroImage.

[102]  C. Braun,et al.  A context for normalizing impulsiveness at work for adults with attention deficit/hyperactivity disorder (combined type). , 2011, Archives of Clinical Neuropsychology.

[103]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[104]  P. Cavanagh,et al.  Cortical fMRI activation produced by attentive tracking of moving targets. , 1998, Journal of neurophysiology.

[105]  John Duncan,et al.  The role of the right inferior frontal gyrus: inhibition and attentional control , 2010, NeuroImage.

[106]  Stuart J. Johnstone,et al.  Neural mechanisms underlying trait impulsivity in non-clinical adults: Stop-signal performance and event-related potentials , 2007, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[107]  R. Constable,et al.  Imaging Response Inhibition in a Stop-Signal Task: Neural Correlates Independent of Signal Monitoring and Post-Response Processing , 2006, The Journal of Neuroscience.

[108]  C. Li,et al.  Activation of the pre-supplementary motor area but not inferior prefrontal cortex in association with short stop signal reaction time – an intra-subject analysis , 2009, BMC Neuroscience.

[109]  Murray B. Stein,et al.  Selective effects of social anxiety, anxiety sensitivity, and negative affectivity on the neural bases of emotional face processing , 2012, NeuroImage.

[110]  R. Dolan,et al.  Distinct spatial frequency sensitivities for processing faces and emotional expressions , 2003, Nature Neuroscience.

[111]  K. Matthews,et al.  Aggression, Impulsivity, and Central Nervous System Serotonergic Responsivity in a Nonpatient Sample , 1998, Neuropsychopharmacology.

[112]  Martin Lepage,et al.  Neural correlates of dual task interference in rapid visual streams: An fMRI study , 2003, Brain and Cognition.

[113]  J. Mattingley,et al.  Fast and slow parietal pathways mediate spatial attention , 2004, Nature Neuroscience.

[114]  Stuart J Johnstone,et al.  Inhibitory motor control in children with attention-deficit/hyperactivity disorder: event-related potentials in the stop-signal paradigm , 2003, Biological Psychiatry.

[115]  Sue-Huei Chen,et al.  Obsessive–compulsiveness and impulsivity in a non-clinical population of adolescent males and females , 2007, Psychiatry Research.

[116]  Vincenzo Varriale,et al.  Impulsivity, intelligence and P300 wave: an empirical study. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[117]  J. Patton,et al.  Toward a Conceptualization of Impulsivity: Components across the Behavioral and Self-Report Domains. , 1987, Multivariate behavioral research.

[118]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

[119]  G. Berns,et al.  Three studies on the neuroeconomics of decision-making when payoffs are real and negative. , 2008, Advances in health economics and health services research.

[120]  D. Gitelman,et al.  The Anterior Insular Cortex Represents Breaches of Taste Identity Expectation , 2011, The Journal of Neuroscience.

[121]  G. Logan,et al.  Impulsivity and Inhibitory Control , 1997 .

[122]  Jens Schwarzbach,et al.  Attentional inhibition of visual processing in human striate and extrastriate cortex , 2003, NeuroImage.

[123]  M. Carrillo-de-la-Peña,et al.  A short-term longitudinal study of impulsivity and antisocial behavior. , 1994, Journal of personality and social psychology.

[124]  H. Levitt Transformed up-down methods in psychoacoustics. , 1971, The Journal of the Acoustical Society of America.

[125]  Derek G. V. Mitchell,et al.  Parsing decision making processes in prefrontal cortex: Response inhibition, overcoming learned avoidance, and reversal learning , 2011, NeuroImage.

[126]  J. Gore,et al.  Neural Correlates of the Attentional Blink , 2000, Neuron.

[127]  Cong Huang,et al.  Neural Correlates of Post-error Slowing during a Stop Signal Task: A Functional Magnetic Resonance Imaging Study , 2008, Journal of Cognitive Neuroscience.