Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-23T19:49:50.787Z Has data issue: false hasContentIssue false
  • English
  • Français

Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback

Published online by Cambridge University Press:  21 January 2014

Amanda E. Guyer ,
Brenda Benson ,
Victoria R. Choate ,
Yair Bar-Haim ,
Koraly Perez-Edgar ,
Johanna M. Jarcho ,
Daniel S. Pine ,
Monique Ernst ,
Nathan A. Fox  and
Eric E. Nelson
Amanda E. Guyer*
Affiliation:
University of California, Davis
Brenda Benson
Affiliation:
National Institute of Mental Health
Victoria R. Choate
Affiliation:
University of Massachusetts, Boston
Yair Bar-Haim
Affiliation:
Tel Aviv University
Koraly Perez-Edgar
Affiliation:
Pennsylvania State University
Johanna M. Jarcho
Affiliation:
National Institute of Mental Health
Daniel S. Pine
Affiliation:
National Institute of Mental Health
Monique Ernst
Affiliation:
National Institute of Mental Health
Nathan A. Fox
Affiliation:
University of Maryland, College Park
Eric E. Nelson
Affiliation:
National Institute of Mental Health
*
Address correspondence and reprint requests to: Amanda E. Guyer, Department of Human Ecology, Center for Mind and Brain, University of California, Davis, 267 Cousteau Place, Davis, CA 95618; E-mail: aeguyer@ucdavis.edu.
Get access Rights & Permissions [Opens in a new window]

Abstract

Behavioral inhibition, a temperament identifiable in infancy, is associated with heightened withdrawal from social encounters. Prior studies raise particular interest in the striatum, which responds uniquely to monetary gains in behaviorally inhibited children followed into adolescence. Although behavioral manifestations of inhibition are expressed primarily in the social domain, it remains unclear whether observed striatal alterations to monetary incentives also extend to social contexts. In the current study, imaging data were acquired from 39 participants (17 males, 22 females; ages 16–18 years) characterized since infancy on measures of behavioral inhibition. A social evaluation task was used to assess neural response to anticipation and receipt of positive and negative feedback from novel peers, classified by participants as being of high or low interest. As with monetary rewards, striatal response patterns differed during both anticipation and receipt of social reward between behaviorally inhibited and noninhibited adolescents. The current results, when combined with prior findings, suggest that early-life temperament predicts altered striatal response in both social and nonsocial contexts and provide support for continuity between temperament measured in early childhood and neural response to social signals measured in late adolescence and early adulthood.

Type
Regular Articles
Information
Development and Psychopathology , Volume 26 , Issue 1 , February 2014 , pp. 229 - 243
Copyright
Copyright © Cambridge University Press 2014 

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

Adolphs, R. (2001). The neurobiology of social cognition. Current Opinion in Neurobiology, 11, 231–239. doi:10.1016/S0959-4388(00)00202-6Google Scholar
Allen, J. P., Porter, M. R., McFarland, F. C., Marsh, P., & McElhaney, K. B. (2005). The two faces of adolescents' success with peers: Adolescent popularity, social adaptation, and deviant behavior. Child Development, 76, 747–760. doi:10.1111/j.1467-8624.2005.00875.xGoogle Scholar
Almas, A. N., Phillips, D. A., Henderson, H. A., Hane, A. A., Degnan, K. A., Moas, O. L., et al. (2011). The relations between infant negative reactivity, nonmaternal childcare, and children's interactions with familiar and unfamiliar peers. Social Development, 20, 718–740. doi:10.1111/j.1467-9507.2011.00605.xCrossRefGoogle ScholarPubMed
Asendorpf, J. B., & Meier, G. H. (1993). Personality effects on children's speech in everyday life: Sociability-mediated exposure and shyness-mediated reactivity to social situations. Journal of Personality and Social Psychology, 64, 1072–1083. doi:10.1037/0022-3514.64.6.1072CrossRefGoogle ScholarPubMed
Atallah, H. E., Lopez-Paniagua, D., Rudy, J. W., & O'Reilly, R. C. (2007). Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nature Neuroscience, 10, 126–131. doi:10.1038/nn1817CrossRefGoogle ScholarPubMed
Bar-Haim, Y., Fox, N. A., Benson, B., Guyer, A. E., Williams, A., Nelson, E. E., et al. (2009). Neural correlates of reward processing in adolescents with a history of inhibited temperament. Psychological Science, 20, 1009–1018. doi:10.1111/j.1467-9280.2009.02401.xCrossRefGoogle ScholarPubMed
Beesdo, K., Bittner, A., Pine, D. S., Stein, M. B., Höfler, M., Lieb, R., et al. (2007). Incidence of social anxiety disorder and the consistent risk for secondary depression in the first three decades of life. Archives of General Psychiatry, 64, 903–912. doi:10.1001/archpsyc.64.8.903Google Scholar
Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., et al. (1997). The Screen for Child Anxiety Related Emotional Disorders (SCARED): Scale construction and psychometric characteristics. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 545–553. doi:10.1097/00004583-199704000-00018Google Scholar
Blakemore, S. J. (2008). The social brain in adolescence. Nature Reviews Neuroscience, 9, 267–277. doi:10.1038/nrn2353Google Scholar
Boivin, M., Hymel, S., & Burkowski, W. M. (1995). The roles of social withdrawal, peer rejection, and victimization by peers in predicting loneliness and depressed mood in childhood. Development and Psychopathology, 7, 765–785. doi:10.1017/S0954579400006830Google Scholar
Brown, B. B. (2004). Adolescents' relationships with peers. In Lerner, R. M. & Steinberg, L. (Eds.), Handbook of adolescent psychology (2nd ed., pp. 363–394). Hoboken, NJ: Wiley.Google Scholar
Burgess, K. B., Wojslawowicz, J. C., Rubin, K. H., Rose-Krasnor, L., & Booth-LaForce, C. (2006). Social information processing and coping strategies of shy/withdrawn and aggressive children: Does friendship matter? Child Development, 77, 371–383. doi:10.1111/j.1467-8624.2006.00876.xCrossRefGoogle ScholarPubMed
Chen, X., DeSouza, A. T., Chen, H., & Wang, L. (2006). Reticent behavior and experiences in peer interactions in Chinese and Canadian children. Developmental Psychology, 42, 656–665. doi:10.1037/0012-1649.42.4.656CrossRefGoogle ScholarPubMed
Chronis-Tuscano, A., Degnan, K. A., Pine, D. S., Perez-Edgar, K., Henderson, H. A., Diaz, Y., et al. (2009). Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 928–935. doi:10.1097/CHI.0b013e3181ae09dfGoogle Scholar
Cicchetti, D., & Rogosch, F. A. (2002). A developmental psychopathology perspective on adolescence. Journal of Consulting and Clinical Psychology, 70, 6–20. doi:10.1037/0022-006X.70.1.6CrossRefGoogle ScholarPubMed
Cicchetti, D., & Thomas, K. M. (2008). Imaging brain systems in normality and psychopathology. Development and Psychopathology, 20, 1023–1027. doi:10.1017/S0954579408000485CrossRefGoogle ScholarPubMed
Cicchetti, D., & Tucker, D. (1994). Development and self-regulatory structures of the mind. Development and Psychopathology, 6, 533–549. doi:10.1017/S0954579400004673Google Scholar
Coplan, R. J., Rubin, K. H., Fox, N. A., Calkins, S. D., & Stewart, S. L. (1994). Being alone, playing alone, and acting alone: Distinguishing among reticence and passive and active solitude among children. Child Development, 65, 129–137.Google Scholar
Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173. doi:10.1006/cbmr.1996.0014Google Scholar
Degnan, K. A., & Fox, N. A. (2007). Behavioral inhibition and anxiety disorders: Multiple levels of a resilience process. Development and Psychopathology, 19, 729–746. doi:10.1017/S0954579407000363CrossRefGoogle ScholarPubMed
Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M., Uddin, L. Q., Shehzad, Z., et al. (2008). Functional connectivity of human striatum: A resting state fMRI study. Cerebral Cortex, 18, 2735–2747. doi:10.1093/cercor/bhn041Google Scholar
Egger, H. L., Pine, D. S., Nelson, E. E., Leibenluft, E., Ernst, M., Towbin, K., et al. (2011). The NIMH Child Emotional Faces Picture Set (NIMH-ChEFS): A new set of children's facial emotion stimuli. International Journal of Methods in Psychiatric Research, 20, 145–156. doi:10.1002/mpr.343Google Scholar
Ernst, M., & Fudge, J. L. (2009). A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes. Neuroscience & Biobehavioral Reviews, 33, 367–382. doi:10.1016/j.neubiorev.2008.10.009Google Scholar
Fox, N. A., Henderson, H. A., Marshall, P. J., Nichols, K. E., & Ghera, M. M. (2005). Behavioral inhibition: Linking biology and behavior within a developmental framework. Annual Review of Psychology, 56, 235–262. doi:10.1146/annurev.psych.55.090902.141532Google Scholar
Fox, N. A., Henderson, H. A., Rubin, K. H., Calkins, S. D., & Schmidt, L. A. (2001). Continuity and discontinuity of behavioral inhibition and exuberance: Psychophysiological and behavioral influences across the first four years of life. Child Development, 72, 1–21. doi:10.1111/1467-8624.00262Google Scholar
Goldsmith, H. H. (1996). Studying temperament via construction of the Toddler Behavior Assessment Questionnaire. Child Development, 67, 218–235. doi:10.1111/j.1467-8624.1996.tb01730CrossRefGoogle ScholarPubMed
Gunther Moor, B., van Leijenhorst, L., Rombouts, S. A., Crone, E. A., & Van der Molen, M. W. (2010). Do you like me? Neural correlates of social evaluation and developmental trajectories. Social Neuroscience, 5, 461–482. doi:10.1080/17470910903526155Google Scholar
Guyer, A. E., Choate, V. R., Detloff, A., Benson, B., Nelson, E. E., Perez-Edgar, K., et al. (2012). Striatal functional alteration during incentive anticipation in pediatric anxiety disorders. American Journal of Psychiatry, 169, 205–212. doi:10.1176/appi.ajp.2011.11010006Google Scholar
Guyer, A. E., Choate, V. R., Pine, D. S., & Nelson, E. E. (2012). Neural circuitry underlying affective response to peer feedback in adolescence. Social Cognitive and Affective Neuroscience, 7, 81–92. doi:10.1093/scan/nsr043Google Scholar
Guyer, A. E., Lau, J. Y., McClure-Tone, E. B., Parrish, J., Shiffrin, N. D., Reynolds, R. C., et al. (2008). Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Archives of General Psychiatry, 65, 1303–1312. doi:10.1001/archpsyc.65.11.1303CrossRefGoogle ScholarPubMed
Guyer, A. E., McClure-Tone, E. B., Shiffrin, N. D., Pine, D. S., & Nelson, E. E. (2009). Probing the neural correlates of anticipated peer evaluation in adolescence. Child Development, 80, 1000–1015. doi:10.1111/j.1467-8624.2009.01313.xCrossRefGoogle ScholarPubMed
Guyer, A. E., Nelson, E. E., Perez-Edgar, K., Hardin, M. G., Roberson-Nay, R., Monk, C. S., et al. (2006). Striatal functional alteration in adolescents characterized by early childhood behavioral inhibition. Journal of Neuroscience, 26, 6399–6405. doi:10.1523/jneurosci.0666-06.2006Google Scholar
Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 4–26. doi:10.1038/npp.2009.129Google Scholar
Hanish, L. D., & Guerra, N. G. (2000). Predictors of peer victimization among urban youth. Social Development, 9, 521–543. doi:10.1111/1467-9507.00141Google Scholar
Haruno, M., & Kawato, M. (2006). Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus–action–reward association learning. Journal of Neurophysiology, 95, 948–959. doi:10.1152/jn.00382.2005Google Scholar
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Science, 4, 223–233. doi:10.1016/S1364-6613(00)01482–0Google Scholar
Hazy, T. E., Frank, M. J., & O'Reilly, R. C. (2010). Neural mechanisms of acquired phasic dopamine responses in learning. Neuroscience & Biobehavioral Reviews, 34, 701–720. doi:10.1016/j.neubiorev.2009.11.019CrossRefGoogle ScholarPubMed
Helfinstein, S. M., Benson, B., Perez-Edgar, K., Bar-Haim, Y., Detloff, A., Pine, D. S., et al. (2011). Striatal responses to negative monetary outcomes differ between temperamentally inhibited and noninhibited adolescents. Neuropsychologia, 49, 479–485. doi:10.1016/j.neuropsychologia.2010.12.015Google Scholar
Helfinstein, S. M., Fox, N. A., & Pine, D. S. (2012). Approach–withdrawal and the role of the striatum in the temperament of behavioral inhibition. Developmental Psychology, 48, 815–826. doi:10.1037/a0026402Google Scholar
Howarth, G. Z., Guyer, A. E., & Perez-Edgar, K. (2013). Young children's affective responses to acceptance and rejection from peers: A computer-based task sensitive to variation in temperamental shyness and gender. Social Development, 22, 146–162. doi:10.1111/sode.12006Google Scholar
Izuma, K., Saito, D. N., & Sadato, N. (2008). Processing of social and monetary rewards in the human striatum. Neuron, 58, 284–294. doi:10.1016/j.neuron.2008.03.020CrossRefGoogle ScholarPubMed
Jarcho, J. M., Fox, N. A., Pine, D. S., Etkin, A., Leibenluft, E., Shechner, T., et al. (2012). The neural correlates of emotion-based cognitive control in adults with early childhood behavioral inhibition. Biological Psychology, 92, 306–314. doi:10.1016/j.biopsycho.2012.09.008Google Scholar
Jones, R. M., Somerville, L. H., Li, J., Ruberry, E. J., Libby, V., Glover, G., et al. (2011). Behavioral and neural properties of social reinforcement learning. Journal of Neuroscience, 31, 13039–13045. doi:10.1523/JNEUROSCI.2972-11.2011Google Scholar
Kagan, J. (1997). Galen's prophecy: Temperament in human nature. Boulder, CO: Westview Press.Google Scholar
Kagan, J., & Fox, N. A. (2007). Biology, culture, and temperamental biases. Handbook of child psychology. Hoboken, NJ: Wiley. doi:10.1002/9780470147658.chpsy0304Google Scholar
Kampe, K. K., Frith, C. D., Dolan, R. J., & Frith, U. (2001). Reward value of attractiveness and gaze. Nature, 413, 589. doi:10.1038/35098149Google Scholar
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., et al. (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children—Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 980–988. doi:10.1097/00004583-199707000-00021Google Scholar
La Greca, A. M., & Lopez, N. (1998). Social anxiety among adolescents: Linkages with peer relations and friendships. Journal of Abnormal Child Psychology, 26, 83–94. doi:10.1023/A:1022684520514Google Scholar
Lau, J. Y., Guyer, A. E., Tone, E. B., Jenness, J., Parrish, J., Pine, D. S., et al. (2011). Neural responses to peer rejection in anxious adolescents: Contributions from the amygdala–hippocampal complex. International Journal of Behavioral Development. doi:10.1177/0165025411406854Google ScholarPubMed
Lorberbaum, J. P., Kose, S., Johnson, M. R., Arana, G. W., Sullivan, L. K., Hamner, M. B., et al. (2004). Neural correlates of speech anticipatory anxiety in generalized social phobia. NeuroReport, 15, 2701–2705.Google Scholar
Marshall, P. J., Reeb, B. C., & Fox, N. A. (2009). Electrophysiological responses to auditory novelty in temperamentally different 9-month-old infants. Developmental Science, 12, 568–582. doi:10.1111/j.1467-7687.2008.00808.xCrossRefGoogle ScholarPubMed
Mattfeld, A. T., Gluck, M. A., & Stark, C. E. (2011). Functional specialization within the striatum along both the dorsal/ventral and anterior/posterior axes during associative learning via reward and punishment. Learning & Memory, 18, 703–711. doi:10.1101/lm.022889.111Google Scholar
McClure, E. B., Monk, C. S., Nelson, E. E., Parrish, J. M., Adler, A., Blair, R. J., et al. (2007). Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Archives of General Psychiatry, 64, 97–106. doi:10.1001/archpsyc.64.1.97Google Scholar
Muranishi, M., Inokawa, H., Yamada, H., Ueda, Y., Matsumoto, N., Nakagawa, M., et al. (2011). Inactivation of the putamen selectively impairs reward history-based action selection. Experimental Brain Research, 209, 235–246. doi:10.1007/s00221-011-2545-yGoogle Scholar
Muris, P., Meesters, C., Merckelbach, H., Sermon, A., & Zwakhalen, S. (1998). Worry in normal children. Journal of the American Academy of Child & Adolescent Psychiatry, 37, 703–710. doi:10.1097/00004583-199807000-00009CrossRefGoogle ScholarPubMed
Nelson, E. E., Leibenluft, E., McClure, E. B., & Pine, D. S. (2005). The social re-orientation of adolescence: A neuroscience perspective on the process and its relation to psychopathology. Psychological Medicine, 35, 163–174. doi:10.1017/S0033291704003915Google Scholar
Perez-Edgar, K., Bar-Haim, Y., McDermott, J. M., Chronis-Tuscano, A., Pine, D. S., & Fox, N. A. (2010). Attention biases to threat and behavioral inhibition in early childhood shape adolescent social withdrawal. Emotion, 10, 349–357. doi:10.1037/a0018486Google Scholar
Perez-Edgar, K., & Fox, N. A. (2005). Temperament and anxiety disorders. Child and Adolescent Psychiatric Clinics of North America, 14, 681–706. doi:10.1016/j.chc.2005.05.008Google Scholar
Perez-Edgar, K., Hardee, J. E., Guyer, A. E., Benson, B. E., Nelson, E. E., Gorodetsky, E., et al. (2013). DRD4 and striatal modulation of the link between childhood behavioral inhibition and adolescent anxiety. Social Cognitive and Affective Neuroscience. doi:10.1093/scan/nst001Google Scholar
Perez-Edgar, K., Roberson-Nay, R., Hardin, M. G., Poeth, K., Guyer, A. E., Nelson, E. E., et al. (2007). Attention alters neural responses to evocative faces in behaviorally inhibited adolescents. Neuroimage, 35, 1538–1546. doi:10.1016/j.neuroimage.2007.02.006Google Scholar
Peters, J., & Buchel, C. (2010). Neural representations of subjective reward value. Behavioural Brain Research, 213, 135–141. doi:10.1016/j.bbr.2010.04.031Google Scholar
Pfeifer, J. H., Lieberman, M. D., & Dapretto, M. (2007). “I know you are but what am I?!” Neural bases of self- and social knowledge retrieval in children and adults. Journal of Cognitive Neuroscience, 19, 1323–1337. doi:10.1162/jocn.2007.19.8.1323Google Scholar
Pine, D. S. (1999). Pathophysiology of childhood anxiety disorders. Biological Psychiatry, 46, 1555–1566. doi:10.1016/S0006-3223(99)00115–8Google Scholar
Redcay, E. (2008). The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism. Neuroscience Biobehavioral Reviews, 32, 123–142. doi:10.1016/j.neubiorev.2007.06.004CrossRefGoogle ScholarPubMed
Rimm-Kaufman, S. E., & Kagan, J. (2005). Infant predictors of kindergarten behavior: The contribution of inhibited and uninhibited temperament types. Behavioral Disorders, 30, 331–347. doi:10.1016/S0193-3973(02)00128–4Google Scholar
Rowe, D. C., & Plomin, R. (1977). Temperament in early childhood. Journal of Personality Assessment, 41, 150–156. doi:10.1207/s15327752jpa4102_5Google Scholar
Rubin, K. H. (1989). The Play Observation Scale (POS). University of Waterloo.Google Scholar
Rubin, K. H., Bukowski, W. M., & Parker, J. G. (2006). Peer interactions, relationships, and groups. In Eisenberg, N. E., Damon, W. E., & Lerner, R. M. E. (Eds.), Handbook of child psychology: Vol. 3. Emotional, and personality development (6th ed., pp. 571–645). Hoboken, NJ: Wiley.Google Scholar
Rubin, K. H., Coplan, R. J., & Bowker, J. C. (2009). Social withdrawal in childhood. Annual Review of Psychology, 60, 141–171. doi:10.1146/annurev.psych.60.110707.163642Google Scholar
Saxe, R. (2006). Uniquely human social cognition. Current Opinion in Neurobiology, 16, 235–239. doi:10.1016/j.conb.2006.03.001CrossRefGoogle ScholarPubMed
Schneier, F. R., Abi-Dargham, A., Martinez, D., Slifstein, M., Hwang, D. R., Liebowitz, M. R., et al. (2009). Dopamine transporters, D2 receptors, and dopamine release in generalized social anxiety disorder. Depression and Anxiety, 26, 411–418. doi:10.1002/da.20543Google Scholar
Schneier, F. R., Liebowitz, M. R., Abi-Dargham, A., Zea-Ponce, Y., Lin, S. H., & Laruelle, M. (2000). Low dopamine D(2) receptor binding potential in social phobia. American Journal of Psychiatry, 157, 457–459. doi:10.1176/appi.ajp.157.3.457Google Scholar
Schultz, W. (2006). Behavioral theories and the neurophysiology of reward. Annual Review of Psychology, 57, 87–115. doi:10.1146/annurev.psych.56.091103.070229Google Scholar
Schwartz, C. E., Wright, C. I., Shin, L. M., Kagan, J., & Rauch, S. L. (2003). Inhibited and uninhibited infants “grown up”: Adult amygdalar response to novelty. Science, 300, 1952–1953. doi:10.1126/science.1083703Google Scholar
Silverman, W. K., La Greca, A. M., & Wasserstein, S. (1995). What do children worry about? Worries and their relation to anxiety. Child Development, 66, 671–686. doi:10.1111/j.1467-8624.1995.tb00897.xGoogle Scholar
Spreckelmeyer, K. N., Krach, S., Kohls, G., Rademacher, L., Irmak, A., Konrad, K., et al. (2009). Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Social Cognitive and Affective Neuroscience, 4, 158–165. doi:10.1093/scan/nsn051Google Scholar
Tarullo, A. R., Mliner, S., & Gunnar, M. R. (2011). Inhibition and exuberance in preschool classrooms: Associations with peer social experiences and changes in cortisol across the preschool year. Developmental Psycholology, 47, 1374–1388. doi:10.1037/a0024093CrossRefGoogle ScholarPubMed
Tiihonen, J., Kuikka, J., Bergström, K., Lepola, U., Koponen, H., & Leinonen, E. (1997). Dopamine reuptake site densities in patients with social phobia. American Journal of Psychiatry, 154, 239–242.Google ScholarPubMed
Trainor, B. C. (2011). Stress responses and the mesolimbic dopamine system: Social contexts and sex differences. Hormones and Behavior, 60, 457–469. doi:10.1016/j.yhbeh.2011.08.013Google Scholar
van Leijenhorst, L., Crone, E. A., & Bunge, S. A. (2006). Neural correlates of developmental differences in risk estimation and feedback processing. Neuropsychologia, 44, 2158–2170. doi:10.1016/j.neuropsychologia.2006.02.002Google Scholar
Voorn, P., Vanderschuren, L. J., Groenewegen, H. J., Robbins, T. W., & Pennartz, C. M. (2004). Putting a spin on the dorsal–ventral divide of the striatum. Trends in Neurosciences, 27, 468–474. doi:10.1016/j.tins.2004.06.006Google Scholar