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Dissociable fronto-striatal functional networks predict choice impulsivity

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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.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

  • 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 7:43–52

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • 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):170–182

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):12315–12320

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • 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):13150–13156

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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):13848–13853

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • 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):2735–2747

    PubMed  Google Scholar 

  • 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):718

    CAS  PubMed  Google Scholar 

  • 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.1602413113

    Article  PubMed  Google Scholar 

  • 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):538

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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):13213–13217

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):12835–12843

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:39–50

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 72:280–286

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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):4886–4895

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):14820–14827

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 200:556–561

    PubMed  Google Scholar 

  • 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/s11682-020-00270-1

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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):2414

    PubMed  PubMed Central  Google Scholar 

  • 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):1695–1702

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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):606–614

    CAS  PubMed  Google Scholar 

  • 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 9:384

    PubMed  PubMed Central  Google Scholar 

  • 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):10298–10310

    PubMed  PubMed Central  Google Scholar 

  • 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.1423095112

    Article  PubMed  Google Scholar 

  • 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):13158–13164

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 134:540–549

    PubMed  Google Scholar 

  • 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):7522–7530

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):643–653

    PubMed  Google Scholar 

  • 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 1261:65–74

    CAS  PubMed  Google Scholar 

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Funding

This work was supported by research grants from the Humanities and Social Science Fund Project of the Ministry of Education (20YJC190018), National natural science foundation of China (31972906), open research fund of the key laboratory of mental health, Institute of Psychology, Chinese Academy of Sciences (KLMH2019K05), and the High-end Foreign expert introduction program (G20190022029).

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Authors and Affiliations

  1. Key Research Base of Humanities and Social Sciences of the Ministry of Education, Academy of Psychology and Behavior, Tianjin Normal University, Tianjin, 300387, China

    Qiang Wang

  2. Faculty of Psychology, Tianjin Normal University, Tianjin, 300387, China

    Qiang Wang

  3. Tianjin Social Science Laboratory of Students’ Mental Development and Learning, Tianjin, 300387, China

    Qiang Wang

  4. Faculty of Psychology, Southwest University, Chongqing, 400715, China

    Chenyu Lv & Qinghua He

  5. CAS Key Laboratory of Mental Health, Institute of Psychology, Beijing, 100101, China

    Qinghua He

  6. National Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China

    Gui Xue

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  1. Qiang Wang
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  2. Chenyu Lv
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  4. Gui Xue
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Correspondence to Qiang Wang, Qinghua He or Gui Xue.

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Wang, Q., Lv, C., He, Q. et al. Dissociable fronto-striatal functional networks predict choice impulsivity. Brain Struct Funct 225, 2377–2386 (2020). https://doi.org/10.1007/s00429-020-02128-0

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