Top

Published in:

01-11-2020 | Original Article

Dissociable fronto-striatal functional networks predict choice impulsivity

Authors: Qiang Wang, Chenyu Lv, Qinghua He, Gui Xue

Published in: Brain Structure and Function | Issue 8/2020

Abstract

Fronto-striatal structural connectivity is associated with choice impulsivity. Yet, to date, whether distinct fronto-striatal functional coupling associates with impulsive choices are largely unknown. Using seed-based resting-state functional MRI (rsfMRI) combined with multivariate pattern analysis (MVPA), the present study aimed to explore the predictions of dissociable frontal–striatal functional connectivity on choice impulsivity in a relatively large sample (N = 429). Adaptive delay-discounting task was utilized to assess choice impulsivity and the striatum was further divided into three subregions including the nucleus accumbens (NAcc), caudate, and putamen. Results revealed that both the functional coupling between the NAcc and the limbic/dorsolateral prefrontal cortex, and between the caudate and the dorsal prefrontal cortex, including the dorsomedial prefrontal cortex (DMPFC), successfully predicted the delay-discounting rate. However, such pattern was not observed in the putamen-prefrontal functional connectivity. These findings suggest fronto-striatal-dependent neural mechanisms of choice impulsivity and further provide a better understanding of the contributions of striatum subregions and their functional connectivities with different areas of prefrontal cortex upon inter-temporal choice.

Available only for authorised users

Alessi S, Petry NM (2003) Pathological gambling severity is associated with impulsivity in a delay discounting procedure. Behav Proc 64(3):345–354

Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9(1):357–381PubMed

Ballard K, Knutson B (2009) Dissociable neural representations of future reward magnitude and delay during temporal discounting. NeuroImage 45(1):143–150PubMed

Bari A, Robbins TW (2013) Inhibition and impulsivity: behavioral and neural basis of response control. Prog Neurobiol 108:44–79PubMed

Bechara A, Damasio AR (2005) The somatic marker hypothesis: a neural theory of economic decision. Games Econ Behav 52(2):336–372

Bechara A, Tranel D, Damasio H (2000) Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 123(11):2189–2202PubMed

Benningfield MM, Blackford JU, Ellsworth ME, Samanez-Larkin GR, Martin PR, Cowan RL, Zald DH (2014) Caudate responses to reward anticipation associated with delay discounting behavior in healthy youth. Dev Cogn Neurosci 7:43–52PubMed

Bickel WK, Odum AL, Madden GJ (1999) Impulsivity and cigarette smoking: delay discounting in current, never, and ex-smokers. Psychopharmacol 146(4):447–454

Cai X, Kim S, Lee D (2011) Heterogeneous coding of temporally discounted values in the dorsal and ventral striatum during intertemporal choice. Neuron 69(1):170–182PubMedPubMedCentral

Chib VS, Rangel A, Shimojo S, O'Doherty JP (2009) Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex. J Neurosci 29(39):12315–12320PubMedPubMedCentral

Christakou A, Brammer M, Rubia K (2011) Maturation of limbic corticostriatal activation and connectivity associated with developmental changes in temporal discounting. NeuroImage 54(2):1344–1354PubMed

Cooper N, Kable JW, Kim BK, Zauberman G (2013) Brain activity in valuation regions while thinking about the future predicts individual discount rates. J Neurosci 33(32):13150–13156PubMedPubMedCentral

Dalley JW, Everitt BJ, Robbins TW (2011) Impulsivity, compulsivity, and top-down cognitive control. Neuron 69(4):680–694PubMed

Damoiseaux J, Rombouts S, Barkhof F, Scheltens P, Stam C, Smith SM, Beckmann C (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103(37):13848–13853PubMed

Daw ND, O’doherty JP, Dayan P, Seymour B, Dolan RJ (2006) Cortical substrates for exploratory decisions in humans. Nature 441(7095):876PubMedPubMedCentral

Dawe S, Gullo MJ, Loxton NJ (2004) Reward drive and rash impulsiveness as dimensions of impulsivity: implications for substance misuse. Addict Behav 29(7):1389–1405PubMed

Di Martino A, Scheres A, Margulies DS, Kelly A, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP (2008) Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 18(12):2735–2747PubMed

Drucker H, Burges CJ, Kaufman L, Smola AJ, Vapnik V Support vector regression machines. In: Advances in neural information processing systems, 1997. pp 155–161

Eagle DM, Humby T, Dunnett SB, Robbins TW (1999) Effects of regional striatal lesions on motor, motivational, and executive aspects of progressive-ratio performance in rats. Behav Neurosci 113(4):718PubMed

Eklund A, Nichols TE, Knutsson H (2016) Cluster failure why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1602413113CrossRefPubMed

Figner B, Knoch D, Johnson EJ, Krosch AR, Lisanby SH, Fehr E, Weber EU (2010) Lateral prefrontal cortex and self-control in intertemporal choice. Nat Neurosci 13(5):538PubMed

Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102(27):9673–9678

Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35(1):4PubMed

Hampton WH, Alm KH, Venkatraman V, Nugiel T, Olson IR (2017) Dissociable frontostriatal white matter connectivity underlies reward and motor impulsivity. NeuroImage 150:336–343PubMedPubMedCentral

Hare TA, Camerer CF, Rangel A (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324(5927):646–648PubMed

Hare TA, Hakimi S, Rangel A (2014) Activity in dlPFC and its effective connectivity to vmPFC are associated with temporal discounting. Front Neurosci 8:50PubMedPubMedCentral

Hariri AR, Brown SM, Williamson DE, Flory JD, de Wit H, Manuck SB (2006) Preference for immediate over delayed rewards is associated with magnitude of ventral striatal activity. J Neurosci 26(51):13213–13217PubMedPubMedCentral

He Q, Xue G, Chen C, Chen C, Lu Z-L, Dong Q (2013) Decoding the neuroanatomical basis of reading ability: a multivoxel morphometric study. J Neurosci 33(31):12835–12843PubMedPubMedCentral

Hu S, Ide JS, Zhang S, Sinha R, Chiang-shan RL (2015) Conflict anticipation in alcohol dependence—a model-based fMRI study of stop signal task. NeuroImage Clin 8:39–50PubMedPubMedCentral

Jimura K, Poldrack RA (2012) Analyses of regional-average activation and multivoxel pattern information tell complementary stories. Neuropsychologia 50(4):544–552PubMed

Johnson MW, Bickel WK (2002) Within-subject comparison of real and hypothetical money rewards in delay discounting. J Exp Anal Behav 77(2):129–146PubMedPubMedCentral

Kable JW, Glimcher PW (2007) The neural correlates of subjective value during intertemporal choice. Nat Neurosci 10(12):1625PubMedPubMedCentral

Koritzky G, He Q, Xue G, Wong S, Xiao L, Bechara A (2013) Processing of time within the prefrontal cortex: recent time engages posterior areas whereas distant time engages anterior areas. NeuroImage 72:280–286PubMed

Kriegeskorte N, Goebel R, Bandettini P (2006) Information-based functional brain mapping. Proc Natl Acad Sci USA 103(10):3863–3868PubMed

Lagorio CH, Madden GJ (2005) Delay discounting of real and hypothetical rewards III: steady-state assessments, forced-choice trials, and all real rewards. Behav Proc 69(2):173–187

Li N, Ma N, Liu Y, He X-S, Sun D-L, Fu X-M, Zhang X, Han S, Zhang D-R (2013) Resting-state functional connectivity predicts impulsivity in economic decision-making. J Neurosci 33(11):4886–4895PubMedPubMedCentral

Luo S, Ainslie G, Giragosian L, Monterosso JR (2009) Behavioral and neural evidence of incentive bias for immediate rewards relative to preference-matched delayed rewards. J Neurosci 29(47):14820–14827PubMedPubMedCentral

Lv C, Wang Q, Chen C, Qiu J, Xue G, He Q (2019) The regional homogeneity patterns of the dorsal medial prefrontal cortex predict individual differences in decision impulsivity. NeuroImage 200:556–561PubMed

Lv C, Wang Q, Chen C, Xue G, He Q (2020) Activation patterns of the dorsal medial prefrontal cortex and frontal pole predict individual differences in decision impulsivity. Brain Imaging Behav. https://doi.org/10.1007/s11682-020-00270-1CrossRefPubMed

McClure SM, Ericson KM, Laibson DI, Loewenstein G, Cohen JD (2007) Time discounting for primary rewards. J Neurosci 27(21):5796–5804PubMedPubMedCentral

McClure SM, Laibson DI, Loewenstein G, Cohen JD (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306(5695):503–507PubMed

Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24(1):167–202PubMed

Mischel W, Shoda Y, Rodriguez MI (1989) Delay of gratification in children. Science 244(4907):933–938PubMed

Morein-Zamir S, Robbins TW (2015) Fronto-striatal circuits in response-inhibition: relevance to addiction. Brain Res 1628:117–129PubMedPubMedCentral

O’Reilly RC (2010) The what and how of prefrontal cortical organization. Trends Neurosci 33(8):355–361PubMedPubMedCentral

Paloyelis Y, Asherson P, Mehta MA, Faraone SV, Kuntsi J (2010) DAT1 and COMT effects on delay discounting and trait impulsivity in male adolescents with attention deficit/hyperactivity disorder and healthy controls. Neuropsychopharmacology 35(12):2414PubMedPubMedCentral

Peper JS et al (2012) Delay discounting and frontostriatal fiber tracts: a combined DTI and MTR study on impulsive choices in healthy young adults. Cereb Cortex 23(7):1695–1702PubMedPubMedCentral

Peters J, Büchel C (2011) The neural mechanisms of inter-temporal decision-making: understanding variability. Trends Cogn Sci 15(5):227–239PubMed

Ramnani N, Owen AM (2004) Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci 5(3):184PubMed

Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306(5695):443–447PubMed

Shin D-J, Jung WH, He Y, Wang J, Shim G, Byun MS, Jang JH, Kim SN, Lee TY, Park HY (2014) The effects of pharmacological treatment on functional brain connectome in obsessive-compulsive disorder. Biol Psychiatry 75(8):606–614PubMed

Tschernegg M, Pletzer B, Schwartenbeck P, Ludersdorfer P, Hoffmann U, Kronbichler M (2015) Impulsivity relates to striatal gray matter volumes in humans: evidence from a delay discounting paradigm. Front Hum Neurosci 9:384PubMedPubMedCentral

van den Bos W, Rodriguez CA, Schweitzer JB, McClure SM (2014) Connectivity strength of dissociable striatal tracts predict individual differences in temporal discounting. J Neurosci 34(31):10298–10310PubMedPubMedCentral

Van Den Bos W, Rodriguez CA, Schweitzer JB, McClure SM (2015) Adolescent impatience decreases with increased frontostriatal connectivity. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1423095112CrossRefPubMed

Venkatraman V, Rosati AG, Taren AA, Huettel SA (2009) Resolving response, decision, and strategic control: evidence for a functional topography in dorsomedial prefrontal cortex. J Neurosci 29(42):13158–13164PubMedPubMedCentral

Wang Q, Chen C, Cai Y, Li S, Zhao X, Zheng L, Zhang H, Liu J, Chen C, Xue G (2016) Dissociated neural substrates underlying impulsive choice and impulsive action. NeuroImage 134:540–549PubMed

Wang Q, Luo S, Monterosso J, Zhang J, Fang X, Dong Q, Xue G (2014) Distributed value representation in the medial prefrontal cortex during intertemporal choices. J Neurosci 34(22):7522–7530PubMedPubMedCentral

Wittmann M, Leland DS, Paulus MP (2007) Time and decision making: differential contribution of the posterior insular cortex and the striatum during a delay discounting task. Exp Brain Res 179(4):643–653PubMed

Xu L, Liang Z-Y, Wang K, Li S, Jiang T (2009) Neural mechanism of intertemporal choice: from discounting future gains to future losses. Brain Res 1261:65–74PubMed

Title: Dissociable fronto-striatal functional networks predict choice impulsivity
Authors: Qiang Wang
Chenyu Lv
Qinghua He
Gui Xue
Publication date: 01-11-2020
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 8/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-020-02128-0

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Dissociable fronto-striatal functional networks predict choice impulsivity

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 8/2020

Aerobic exercise increases sprouting angiogenesis in the male rat motor cortex

Changes in auditory cortical thickness following music training in children: converging longitudinal and cross-sectional results

Effect of BDNF Val66Met on hippocampal subfields volumes and compensatory interaction with APOE-ε4 in middle-age cognitively unimpaired individuals from the ALFA study

Abnormal dynamic resting-state brain network organization in auditory verbal hallucination

Volumetric analysis and morphological assessment of the ascending olfactory pathway in an elasmobranch and a teleost using diceCT

Brain connections derived from diffusion MRI tractography can be highly anatomically accurate—if we know where white matter pathways start, where they end, and where they do not go