Neurobiological correlates of impulsivity in healthy adults: Lower prefrontal gray matter volume and spontaneous eye-blink rate but greater resting-state functional connectivity in basal ganglia-thalamo-cortical circuitry

Abstract

Studies consistently implicate aberrance of the brain’s reward-processing and decision-making networks in disorders featuring high levels of impulsivity, such as attention-deficit hyperactivity disorder, substance use disorder, and psychopathy. However, less is known about the neurobiological determinants of individual differences in impulsivity in the general population. In this study of 105 healthy adults, we examined relationships between impulsivity and three neurobiological metrics – gray matter volume, resting-state functional connectivity, and spontaneous eye-blink rate, a physiological indicator of central dopaminergic activity. Impulsivity was measured both by performance on a task of behavioral inhibition (go/no-go task) and by self-ratings of attentional, motor, and non-planning impulsivity using the Barratt Impulsiveness Scale (BIS-11). Overall, we found that less gray matter in medial orbitofrontal cortex and paracingulate gyrus, greater resting-state functional connectivity between nodes of the basal ganglia-thalamo-cortical network, and lower spontaneous eye-blink rate were associated with greater impulsivity. Specifically, less prefrontal gray matter was associated with higher BIS-11 motor and non-planning impulsivity scores, but was not related to task performance; greater correlated resting-state functional connectivity between the basal ganglia and thalamus, motor cortices, and prefrontal cortex was associated with worse no-go trial accuracy on the task and with higher BIS-11 motor impulsivity scores; lower spontaneous eye-blink rate was associated with worse no-go trial accuracy and with higher BIS-11 motor impulsivity scores. These data provide evidence that individual differences in impulsivity in the general population are related to variability in multiple neurobiological metrics in the brain’s reward-processing and decision-making networks.

Volume of motor area predicts motor impulsivity

“…[Colour figure can be viewed at wileyonlinelibrary.com] was correlated with high motor impulsivity (Matsuo et al, 2009). These heterogeneous findings might be attributed to age difference of different samples (Ide et al, 2017;Korponay et al, 2017;Kubera et al, 2018) and the small-volume correction approach used in previous studies (Cho et al, 2013;Matsuo et al, 2009), which may lead to hypothesis-driven results. This issue indicates the importance of identifying the morphometric neural basis of impulsivity at a whole-brain level.…”

“…These three dimensions have shown disassociated effects on cognitive functions in many studies, indicating that their underlying mechanisms are isolated to some extent (for a review, see Stanford et al, 2009). Previous neuroimaging studies have found alterations in neural pathways of mesocorticostriatal (Dalley, Mar, Economidou, &Robbins, 2008;Korponay, Dentico, Kral, Ly, &Kruis, 2017;Shannon et al, 2011;Wolf et al, 2011) and corticolimbic networks (Brown, Manuck, Flory, &Hariri, 2006;Cho et al, 2013;Liston, Cohen, Teslovich, Levenson, &Casey, 2011;Xie et al, 2011); as well as dysfunctions in certain brain areas such as the IFG (Aron, Fletcher, Bullmore, Sahakian, &Robbins, 2003;Goya-Maldonado et al, 2010), ACC (Cho et al, 2013;Lee et al, 2013;Matsuo et al, 2009), and OFC (Crunelle et al, 2014;Matsuo et al, 2009;Schilling et al, 2012) in individuals with high impulsivity. Both overlapping and distinct neural underpinnings of the three dimensions of impulsiveness have been observed in morphometric studies.…”

“…Both overlapping and distinct neural underpinnings of the three dimensions of impulsiveness have been observed in morphometric studies. Decreased cortical thickness in the pericalcarine gyrus (Kubera et al, 2018) and increased parieto-occipital cortical volume (Ide, Tung, Yang, Tseng, &amp;Li, 2017) have been reported to be associated with non-planning but not motor impulsivity in healthy young adults, while prefrontal volumes were inversely correlated with motor and non-planning impulsivity in a relatively older sample (Korponay et al, 2017). Another study has reported that smaller right OFC was associated with non-planning impulsivity, while smaller left OFC F I G U R E 1 The brain regions revealed by multiple regression analysis of motor impulsiveness on GM volumes (p < 0.001 uncorrected at voxel-level with p < 0.05 FWE-corrected at cluster level).…”

Frontal cortical thickness correlates positively with impulsivity in early psychosis male patients

“…Our brain imaging results are in line with some previous findings showing that orbito-frontal volume relates positively to aggression in schizophrenia (Hoptman et al, 2005), orbito-frontal cortex volume relates positively to motor impulsivity in a non-psychotic psychiatric population (Antonucci et al, 2006) and grey matter volume of superior and middle frontal regions correlates positively with impulsiveness score in healthy controls (Gardini, Cloninger, & Venneri, 2009). The finding of a positive association between impulsivity and frontal cortical thickness may seem rather counterintuitive and is in contrast with studies where impulsive behaviour is linked to reduced grey matter volume in healthy controls (Korponay et al, 2017) or reduced cortical thickness in schizophrenia (Hoptman et al, 2014); for review see (Ouzir, 2013). The normal process of brain development and maturation involves a phase of cortical thickness increase during childhood, followed by cortical thinning during adolescence and adulthood, which plays an important role in the refinement of neural circuits (Giedd et al, 1999;Shaw et al, 2008).…”

Static and Dynamic Aspects of Cerebro-Cerebellar Functional Connectivity are Associated with Self-reported Measures of Impulsivity: A Resting-State fMRI Study

“…One study has reported significant associations between elevated impulsivity and decreased FC between prefrontal control and sub-cortical appetitive drive regions in healthy young individuals (Davis et al, 2012). Another study has reported significant associations between basal ganglia-thalamo-cortical FC and BIS-11 motor and non-planning impulsivity in healthy adults (Korponay et al, 2017). In addition, fronto-striatal FC has been observed to be strongly associated with BAS fun-seeking (Angelides et al, 2017).…”