Hostname: page-component-6d856f89d9-jhxnr Total loading time: 0 Render date: 2024-07-16T03:34:11.318Z Has data issue: false hasContentIssue false

Development of a cortical delay discounting assay: a potential biomarker of externalizing disorders

Published online by Cambridge University Press:  25 June 2021

Naomi Sadeh*
Affiliation:
Department of Psychological and Brain Sciences, University of Delaware, Newark, DE 19716, USA
Rickie Miglin
Affiliation:
Department of Psychological and Brain Sciences, University of Delaware, Newark, DE 19716, USA
Nadia Bounoua
Affiliation:
Department of Psychological and Brain Sciences, University of Delaware, Newark, DE 19716, USA
Ana Sheehan
Affiliation:
Department of Psychological and Brain Sciences, University of Delaware, Newark, DE 19716, USA
Jeffrey M. Spielberg
Affiliation:
Department of Psychological and Brain Sciences, University of Delaware, Newark, DE 19716, USA
*
Author for correspondence: Naomi Sadeh, Email: nsadeh@udel.edu

Abstract

Background

People who tend to impulsively choose smaller, sooner rewards over larger, later rewards are at increased risk for addiction and psychiatric disorders. A neurobiological measure of the tendency to overvalue immediate gratification could facilitate the study of individuals who are susceptible to these mental disorders. The objective of this research was to develop a cortical assay of impulsive choice for immediate rewards.

Methods

A cortex-based assay of impulsive choice was developed using 1105 healthy adults from the Human Connectome Project, and then cross-validated in two independent samples of adults with elevated rates of psychiatric disorders.

Results

Study 1: Cortical delay discounting (C-DD) was developed using a multivariate additive model of gray matter thickness across both hemispheres. Higher C-DD corresponded to thinner cortex and greater impulsive choice for immediate rewards. It also predicted cannabis use beyond established risk factors for drug use, including familial substance use, childhood conduct problems, personality traits, and cognitive functioning. Study 2: C-DD replicated the association with delay discounting performance from study 1. Structural equation modeling showed C-DD covaried with symptoms of externalizing, but not internalizing disorders. Study 3: C-DD positively predicted future delay discounting behavior (6–34 months later).

Conclusions

Across three studies, a cortical assay of impulsive choice evidenced consistent associations with drug use and delay discounting task performance. It was also uniquely associated with psychiatric disorders that share impulsivity as a core feature. Together, findings support the utility of C-DD as a neurobiological assay of impulsive decision-making and a possible biomarker of externalizing disorders.

Type
Original Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amlung, M., Marsden, E., Holshausen, K., Morris, V., Patel, H., Vedelago, L., & …McCabe, R. E. (2019). Delay discounting as a transdiagnostic process in psychiatric disorders: A meta-analysis. JAMA Psychiatry, 76(11), 11761186.CrossRefGoogle ScholarPubMed
Amlung, M., Vedelago, L., Acker, J., Balodis, I., & MacKillop, J. (2017). Steep delay discounting and addictive behavior: A meta-analysis of continuous associations. Addiction, 112(1), 5162.CrossRefGoogle ScholarPubMed
Barry, A. B., Koeppel, J. A., & Ho, B. C. (2020). Impulsive decision making, brain cortical thickness and familial schizophrenia risk. Schizophrenia Research, 220, 5460.CrossRefGoogle ScholarPubMed
Baskin-Sommers, A. R., Curtin, J. J., & Newman, J. P. (2015). Altering the cognitive-affective dysfunctions of psychopathic and externalizing offender subtypes with cognitive remediation. Clinical Psychological Science, 3(1), 4557.CrossRefGoogle ScholarPubMed
Bernhardt, B. C., Smallwood, J., Tusche, A., Ruby, F. J., Engen, H. G., Steinbeis, N., & Singer, T. (2014). Medial prefrontal and anterior cingulate cortical thickness predicts shared individual differences in self-generated thought and temporal discounting. NeuroImage, 90, 290297.CrossRefGoogle ScholarPubMed
Bickel, W. K., Athamneh, L. N., Basso, J. C., Mellis, A. M., DeHart, W. B., Craft, W. H., & Pope, D. (2019). Excessive discounting of delayed reinforcers as a trans-disease process: Update on the state of the science. Current Opinion in Psychology, 30, 5964.CrossRefGoogle ScholarPubMed
Bilker, W. B., Hansen, J. A., Brensinger, C. M., Richard, J., Gur, R. E., & Gur, R. C. (2012). Development of abbreviated nine-item forms of the Raven's standard progressive matrices test. Assessment, 19(3), 354369.CrossRefGoogle ScholarPubMed
Bjork, J. M., Momenan, R., & Hommer, D. W. (2009). Delay discounting correlates with proportional lateral frontal cortex volumes. Biological Psychiatry, 65(8), 710713.CrossRefGoogle ScholarPubMed
Bobova, L., Finn, P., Rickert, M., & Lucas, J. (2009). Disinhibitory psychopathology and delay discounting in alcohol dependence: Personality and cognitive correlates. Experimental and Clinical Psychopharmacology, 17(1), 5161.CrossRefGoogle ScholarPubMed
Bucholz, K. K., Cadoret, R., Cloninger, C. R., Dinwiddie, S. H., Hesselbrock, V. M., Nurnberger, J. I. Jr., & …Schuckit, M. A. (1994). A new, semi-structured psychiatric interview for use in genetic linkage studies: A report on the reliability of the SSAGA. Journal of Studies on Alcohol, 55(2), 149158.CrossRefGoogle ScholarPubMed
Cho, S. S., Pellecchia, G., Aminian, K., Ray, N., Segura, B., Obeso, I., & Strafella, A. P. (2013). Morphometric correlation of impulsivity in medial prefrontal cortex. Brain Topography, 26(3), 479487.CrossRefGoogle ScholarPubMed
Costa, P. T., & McCrae, R. R. (1989). NEO five-factor inventory (NEO-FFI). Odessa, FL: Psychological Assessment Resources, 3.Google Scholar
Destrieux, C., Fischl, B., Dale, A., & Halgren, E. (2010). Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage, 53(1), 115.CrossRefGoogle ScholarPubMed
Dombrovski, A. Y., Siegle, G. J., Szanto, K., Clark, L., Phil, D., Reynolds, C. F. III, & Aizenstein, H. (2012). The temptation of suicide: Striatal gray matter, discounting of delayed rewards, and suicide attempts in late-life depression. Psychological Medicine, 42(6), 12031215.CrossRefGoogle ScholarPubMed
Finn, P. R., Gunn, R. L., & Gerst, K. R. (2015). The effects of a working memory load on delay discounting in those with externalizing psychopathology. Clinical Psychological Science, 3(2), 202214.CrossRefGoogle ScholarPubMed
First, M. B., Williams, J. B. W., Karg, R. S., & Spitzer, R. L. (2015). Structured clinical interview for DSM-5—Research version (SCID-5 for DSM-5, research version; SCID-5-RV). Arlington, VA: American Psychiatric Association, pp. 1–94.Google Scholar
Glasser, M. F., Sotiropoulos, S. N., Wilson, J. A., Coalson, T. S., Fischl, B., & Andersson, J. L., … & Wu-Minn HCP Consortium. (2013). The minimal preprocessing pipelines for the human connectome project. NeuroImage, 80, 105124.CrossRefGoogle ScholarPubMed
Han, X., Jovicich, J., Salat, D., van der Kouwe, A., Quinn, B., Czanner, S., & …Fischl, B. (2006). Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer. NeuroImage, 32(1), 180194.CrossRefGoogle ScholarPubMed
Iacono, W. G., Malone, S. M., & McGue, M. (2008). Behavioral disinhibition and the development of early-onset addiction: Common and specific influences. Annual Review of Clinical Psychology, 4, 325348.CrossRefGoogle ScholarPubMed
Kendler, K. S., Prescott, C. A., Myers, J., & Neale, M. C. (2003). The structure of genetic and environmental risk factors for common psychiatric and substance use disorders in men and women. Archives of General Psychiatry, 60(9), 929937.CrossRefGoogle ScholarPubMed
Krueger, R.F., Markon, K., Patrick, C., Benning, S., & Kramer, M. (2007). Linking antisocial behavior, substance use, and personality: An integrative quantitative model of the adult externalizing Spectrum. Journal of Abnormal Psychology, 116(4), 645666.CrossRefGoogle ScholarPubMed
Krueger, R. F., & South, S. C. (2009). Externalizing disorders: Cluster 5 of the proposed meta-structure for DSM-V and ICD-11: Paper 6 of 7 of the thematic section: ‘A proposal for a meta-structure for DSM-V and ICD-11’. Psychological Medicine, 39(12), 20612070.CrossRefGoogle Scholar
Loganathan, K., Lv, J., Cropley, V., Ho, E. T. W., & Zalesky, A. (2021). Associations between delay discounting and connectivity of the valuation-control system in healthy young adults. Neuroscience, 452, 295310.CrossRefGoogle ScholarPubMed
Mazur, J. E. (1987). An adjusting procedure for studying delayed reinforcement. Commons, ML.; Mazur, JE.; Nevin, JA, pp. 5573.Google Scholar
McClure, S. M., Laibson, D. I., Loewenstein, G., & Cohen, J. D. (2004). Separate neural systems value immediate and delayed monetary rewards. Science, 306(5695), 503507.CrossRefGoogle ScholarPubMed
Noble, S., Spann, M. N., Tokoglu, F., Shen, X., Constable, R. T., & Scheinost, D. (2017). Influences on the test–retest reliability of functional connectivity MRI and its relationship with behavioral utility. Cerebral Cortex, 27(11), 54155429.CrossRefGoogle ScholarPubMed
Noda, Y., Barr, M. S., ElSalhy, M., Masuda, F., Tarumi, R., Ogyu, K., … & Mimura, M. (2020). Neural correlates of delay discount alterations in addiction and psychiatric disorders: a systematic review of magnetic resonance imaging studies. Progress in Neuro–Psychopharmacology and Biological Psychiatry, 99, 109822.CrossRefGoogle ScholarPubMed
Odum, A. L. (2011a). Delay discounting: I'm a k, you're a k. Journal of the Experimental Analysis of Behavior, 96(3), 427439.CrossRefGoogle Scholar
Odum, A. L. (2011b). Delay discounting: Trait variable?. Behavioural Processes, 87(1), 19.CrossRefGoogle ScholarPubMed
Owens, M. M., Gray, J. C., Amlung, M. T., Oshri, A., Sweet, L. H., & MacKillop, J. (2017). Neuroanatomical foundations of delayed reward discounting decision making. NeuroImage, 161, 261270.CrossRefGoogle ScholarPubMed
Patrick, C. J., Venables, N. C., Yancey, J. R., Hicks, B. M., Nelson, L. D., & Kramer, M. (2013). A construct-network approach to bridging diagnostic and physiological domains: Application to assessment of externalizing psychopathology. Journal of Abnormal Psychology, 122(3), 902916.CrossRefGoogle ScholarPubMed
Petker, T., Owens, M. M., Amlung, M. T., Oshri, A., Sweet, L. H., & MacKillop, J. (2019). Cannabis involvement and neuropsychological performance: Findings from the human connectome project. Journal of Psychiatry & Neuroscience, 44(6), 414422.CrossRefGoogle ScholarPubMed
Sadeh, N., Spielberg, J. M., Logue, M. W., Hayes, J. P., Wolf, E. J., McGlinchey, R. E., & …Miller, M. W. (2019). Linking genes, circuits, and behavior: Network connectivity as a novel endophenotype of externalizing. Psychological Medicine, 49(11), 19051913.CrossRefGoogle ScholarPubMed
Serafini, G., Canepa, G., Adavastro, G., Nebbia, J., Belvederi Murri, M., Erbuto, D., … Amore, M. (2017). The relationship between childhood maltreatment and non-suicidal self-injury: A systematic review. Frontiers in Psychiatry, 8, 149.CrossRefGoogle ScholarPubMed
Strickland, J. C., Lee, D. C., Vandrey, R., & Johnson, M. W. (2020). A systematic review and meta-analysis of delay discounting and cannabis use. Experimental and Clinical Psychopharmacology. Advanced online publication.Google ScholarPubMed
Sugrue, L. P., & Desikan, R. S. (2019). What are polygenic scores and why are they important?. JAMA, 321(18), 18201821.CrossRefGoogle ScholarPubMed
van der Kouwe, A. J., Benner, T., Salat, D. H., & Fischl, B. (2008). Brain morphometry with multiecho MPRAGE. NeuroImage, 40(2), 559569.CrossRefGoogle ScholarPubMed
Van Essen, D. C., Ugurbil, K., Auerbach, E., Barch, D., Behrens, T. E., & Bucholz, R., … & WU-Minn HCP Consortium. (2012). The human connectome project: A data acquisition perspective. NeuroImage, 62(4), 22222231.CrossRefGoogle ScholarPubMed
Weintraub, S., Dikmen, S. S., Heaton, R. K., Tulsky, D. S., Zelazo, P. D., Bauer, P. J., & …Gershon, R. C. (2013). Cognition assessment using the NIH toolbox. Neurology, 80(11 Suppl 3), S54S64.CrossRefGoogle ScholarPubMed
Yeh, Y. H., Myerson, J., & Green, L. (2021). Delay discounting, cognitive ability, and personality: What matters?. Psychonomic Bulletin & Review, 28(2), 686694.CrossRefGoogle ScholarPubMed
Yoon, J. H., Higgins, S. T., Heil, S. H., Sugarbaker, R. J., Thomas, C. S., & Badger, G. J. (2007). Delay discounting predicts postpartum relapse to cigarette smoking among pregnant women. Experimental and Clinical Psychopharmacology, 15(2), 176186.CrossRefGoogle ScholarPubMed
Supplementary material: File

Sadeh et al. supplementary material

Sadeh et al. supplementary material

Download Sadeh et al. supplementary material(File)
File 20 KB