Behavioral and neural correlates of delay of gratification 40 years later B. J. Caseya,1, Leah H. Somervillea, Ian H. Gotlibb, Ozlem Aydukc, Nicholas T. Franklina, Mary K. Askrend, John Jonidesd, Marc G. Bermand, Nicole L. Wilsone, Theresa Teslovicha, Gary Gloverf, Vivian Zayasg, Walter Mischelh,1, and Yuichi Shodae,1 aSackler Institute for Developmental Psychobiology, Weill Cornell Medical College, New York, NY 10065 bDepartment of Psychology, Stanford University, Stanford, CA 94305 cDepartment of Psychology, University of California, Berkeley, CA 94720 dDepartment of Psychology, University of Michigan, Ann Arbor, MI 48109 eDepartment of Psychology, University of Washington, Seattle, WA 98195 fLucas Imaging Center, Department of Radiology, Stanford University School of Medicine, Stanford, CA 94305 gDepartment of Psychology, Cornell University, Ithaca, NY 14853 and hDepartment of Psychology, Columbia University, New York, NY 10027 Edited* by Michael Posner, University of Oregon, Eugene, OR, and approved July 26, 2011 (received for review May 27, 2011) We examined the neural basis of self-regulation in individuals from a cohort of preschoolers who performed the delay-of- gratification task 4 decades ago. Nearly 60 individuals, now in their mid-forties, were tested on ���hot��� and ���cool��� versions of a go/ nogo task to assess whether delay of gratification in childhood predicts impulse control abilities and sensitivity to alluring cues (happy faces). Individuals who were less able to delay gratification in preschool and consistently showed low self-control abilities in their twenties and thirties performed more poorly than did high delayers when having to suppress a response to a happy face but not to a neutral or fearful face. This finding suggests that sensi- tivity to environmental hot cues plays a significant role in individ- uals��� ability to suppress actions toward such stimuli. A subset of these participants (n = 26) underwent functional imaging for the first time to test for biased recruitment of frontostriatal circuitry when required to suppress responses to alluring cues. Whereas the prefrontal cortex differentiated between nogo and go trials to a greater extent in high delayers, the ventral striatum showed exaggerated recruitment in low delayers. Thus, resistance to temp- tation as measured originally by the delay-of-gratification task is a relatively stable individual difference that predicts reliable biases in frontostriatal circuitries that integrate motivational and control processes. reward | behavioral suppression | functional MRI | inferior frontal gyrus | longitudinal Tessential he ability to resist temptation in favor of long-term goals is an component of individual, societal, and economical success. Developmentally, this ability has been assessed by measuring how long a young child can resist an immediate re- ward (e.g., a cookie) in favor of a larger, later reward (e.g., two cookies) (1). Even as adults we vary in our ability to resist temptations. Alluring situations can diminish our control (2���4) what serves as an alluring situation that requires a capacity to control our impulses, however, changes as a function of age (e.g., from cookies to social acceptance). In the present study we ex- amined the extent to which individual differences in delay of gratification assessed when participants were in preschool and in their 20s and 30s predict control over impulses and sensitivity to social cues at the behavioral and neural level when the partic- ipants were in their 40s. Delay of gratification depends importantly on cognitive con- trol (5). Cognitive control refers to the ability to suppress com- peting inappropriate thoughts or actions in favor of appropriate ones (6���11). Previously, we have shown that performance on the delay-of-gratification task in childhood predicts the efficiency with which the same individuals perform a cognitive control task (the go/nogo task) as adolescents and young adults (5). Indi- viduals who as preschoolers directed their attention toward re- warding aspects of the classic delay-of-gratification situation, such as focusing on the cookies (high-temptation-focus group), had more difficulty suppressing inappropriate actions than did their low-temptation-focus counterparts, especially for the most difficult trials. Difficulty was manipulated by increasing the num- ber of ���go��� trials preceding a ���nogo��� trial, thus making the ���go��� response more salient and automated. Differences between the high- and low-temptation-focus groups increased as the number of preceding ���go��� trials increased, with the high-temptation-focus group having more difficulty, reflected in slower response times, suppressing responses. These findings suggest that performance in preschool delay of gratification may predict the capacity, in adulthood, to control thoughts and actions, as reflected in per- formance on cognitive control tasks, and that the ability to control one���s thoughts and actions can vary by the potency of interfering information (12). Likewise, alluring or social contexts can diminish self-control (4, 13, 14). Early experiments on delay of gratification demonstrated that part of the contextual effect was due to the different cognitive strategies that individuals used. For example, ���cooling��� the hot, appealing, or appetitive features of tempting stimuli by reap- praisal or reframing strategies to focus on their cool, cognitive features (e.g., to envision the marshmallow as a cloud or a little cotton ball, rather than as a sweet, delectable treat) has been shown to be highly effective in enhancing delay of gratification (e.g., 1, 15���17). The same preschool child who yielded immedi- ately to the temptation by representing the hot, appetitive fea- tures of the reward (e.g., its yummy, sweet, chewy taste) could wait for long periods for the same tempting stimulus by focusing on its cool qualities (e.g., its shape). At the same time, there seem to be important, naturally existing individual differences in the spontaneous use of such strategies (e.g., 5, 18). Indeed, Metcalfe and Mischel (2) proposed ���cool��� and ���hot��� systems to explain the dynamics of resisting temptation during the delay-of-gratification task. These two interacting neuro- cognitive systems are implicated in self-control. Whereas the first, a ���cool��� system, involves cognitive control-related neural circuitry, the second, a ���hot��� system (19), involves desires and emotions that are under stimulus control and are associated with emotional brain regions. Recent brain imaging studies have provided evidence for dissociable brain systems related to im- mediate over long-term choice behavior consistent with the no- Author contributions: B.J.C., O.A., J.J., M.G.B., N.L.W., G.G., V.Z., W.M., and Y.S. designed research I.H.G., O.A., M.K.A., J.J., M.G.B., N.L.W., W.M., and Y.S. performed research B.J.C., N.L.W., T.T., G.G., V.Z., W.M., and Y.S. contributed new reagents/experimental tools B.J.C., L.H.S., N.T.F., N.L.W., T.T., W.M., and Y.S. analyzed data and B.J.C., L.H.S., I.H.G., O.A., J.J., M.G.B., N.L.W., V.Z., W.M., and Y.S. wrote the paper. The authors declare no conflict of interest. *This Direct Submission article had a prearranged editor. Freely available online through the PNAS open access option. 1 To whom correspondence may be addressed. E-mail: bjc2002@med.cornell.edu, wm@ psych.columbia.edu, or yshoda@u.washington.edu. www.pnas.org/cgi/doi/10.1073/pnas.1108561108 PNAS Early Edition | 1 of 6 PSYCHOLOGICAL AND COGNITIVE SCIENCES

tion of interacting ���hot��� and ���cool��� systems. Specifically, whereas top-down prefrontal regions have been shown to be involved in cognitive control during delay of rewards, limbic or emotional brain regions have been shown to be associated with more im- mediate choices (20���24). Complementary imaging studies have shown that a region of the prefrontal cortex, the inferior frontal gyrus, is critically involved in resolving interference among competing actions [e.g., to go or not to go (10, 25)] and among competing representations in memory (e.g., 11). In each case, prepotent information interferes with other goal-specific in- formation, thus requiring cognitive control processes to resolve the interference. In the present longitudinal study, we manipulated the alluring qualities of targets in an impulse control task to examine be- havioral and neural correlates of delay of gratification using functional magnetic resonance imaging (fMRI). Participants were individuals whose ability to delay gratification was tested as 4-y-olds on the original delay-of-gratification task and whose self- control abilities remained consistent in follow-up assessments. Two experiments were conducted to investigate the ability of these individuals, now in their 40s, to refrain from responding to alluring cues. We developed two tasks to examine impulse con- trol���one in the presence of neutral (���cool���) stimuli and one containing compelling (���hot���) stimuli. Because marshmallows and cookies are unlikely to be as rewarding to individuals now as adults as they were when they were young children, we used the social cues of faces with emotional expressions (happy faces relative to neutral and fearful faces), shown to bias behavior similarly to secondary reinforcers (4, 13, 26). Experiment 1 tested whether individuals who were less able to delay gratifi- cation as children and young adults (low delayers) would, as adults in their 40s, show less impulse control in suppression of a response to ���hot��� relative to ���cool��� cues. In experiment 2, we used fMRI to examine neural correlates of delay of gratification. We hypothesized that participants with consistently low levels of self-control from young childhood to early adulthood (low delayers), compared with their consistently high-control counterparts, would be characterized by diminished activity in the right prefrontal cortex, implicated in response inhibition (13, 27���29), and by amplified activity in the ventral striatum, implicated in processing of positive or rewarding cues (13, 26, 30). Result and Discussion Experiment 1 Results. In experiment 1, 59 participants classified as low or high delayers (Table 1) completed a behavioral version of the ���hot��� and ���cool��� impulse control tasks. Reaction times for trials that required a response (���go��� trials) and accuracy for ���go��� and ���nogo��� trials were compared by delay group and task. Reaction times. There were no effects of delay group on reaction time measures to correct ���go��� trials [main effect of group, F (1,57) = 2.23, P 0.1 group �� task interaction, F(1,57) = 0.002, P 0.9]. Accuracy. Participants performed with a high level of accuracy for correctly responding to ���go��� trials during both the ���cool��� (99.8% correct) and ���hot��� tasks (99.5% correct). Low and high delayers performed with comparable accuracy on ���go��� trials [neither the main effect of group, F(1,57) = 1.08, P 0.3, nor the interaction of group and task, F(1,57) = 0.05, P 0.8, was significant]. Accuracy for ���nogo��� trials was more variable [mean false alarm rate for ���cool��� task, 9.96% for ���hot��� task, 12.2% main effect of task, F(1,57) = 7.89, P = 0.007, ��2partial = 0.122] and yielded a significant interaction of group and task [F(1,57) = 4.312, P = 0.042, ��2partial = 0.070 Fig. 1]. Whereas low and high delayers performed comparably on the ���cool��� task [t(57) = -0.24, P 0.8], the low delayers trended toward performing more poorly on the ���hot��� task than did the high delayers [t(57) = 1.64, P = 0.11, d = 0.43]. Further, only the low delay group showed a significant decrement in performance for the ���hot��� trials relative to the ���cool��� trials [t(26) = 3.09, P = 0.005, d = 0.89 high delay group P 0.5]. Additional planned analyses separated ���hot��� task ���nogo��� trials into fear and happy sub- categories. The decrement in performance for low delayers was driven largely by commission errors on the happy ���nogo��� trials [low delayers, 15.7% errors high delayers, 11.2% errors t(57) = 2.06, P = 0.044, d = 0.55], whereas low and high delaying groups performed at equivalent levels of accuracy for the fear ���nogo��� trials [12.0% and 10.4%, respectively, t(57) = 0.804, P 0.4]. Experiment 1 Discussion. In this experiment the go/nogo task produced differences between the two delay groups only in the presence of emotional (���hot���) cues. Specifically, individuals who, as a group, had more difficulty delaying gratification at 4 y of age showed more difficulty as adults in suppressing responses to happy faces. The findings are consistent with previous work suggesting that the capacity to resist temptation varies by con- text the more tempting the choice for the individual, the more predictive are the individual differences in people���s ability to regulate their behavior (e.g., 12). Thus, behavioral correlates of delay ability are a function not only of cognitive control but also of the compelling nature of the stimuli that must be suppressed. Because behavioral differences between the low and high delayers only emerged on the ���hot��� task, we scanned participants during this task in experiment 2. Experiment 2 Results. Reaction times. As with the behavioral find- ings outside of the scanner, the two delay groups did not differ significantly in reaction times to correct ���go��� trials [t(24) = 0.81, P 0.4]. Accuracy. Overall, accuracy rates for the ���hot��� go/nogo task in the scanner were uniformly high for ���go��� trials (mean 98.2% correct hits), with more variable performance to ���nogo��� trials (12.4% false alarm rate). Differences between the two delay groups in ���nogo��� accuracy were consistent with the observed differences in the ���hot��� task performance in experiment 1, with low-delay participants committing more false alarms than high-delay par- ticipants (low delayers, 14.5% high delayers, 10.9% Fig. 1, Right). This performance difference, however, did not reach statistical significance [t(24) = 1.08, P = 0.29, d = 0.44], likely Table 1. Subject demographics Group n Female (n) Age (y) Age 4 y delay score Adult self-report Raven���s score* Experiment 1 sample High delaying 32 20 44.6 �� 2.1 332.3 �� 147.0 7.61 �� 0.54 Low delaying 27 16 44.3 �� 1.6 -284.2 �� 145.2 5.91 �� 1.04 Experiment 2 sample High delaying 15 10 44.8 �� 1.8 304.2 �� 145.2 7.39 �� 0.45 25.5 �� 5.0 Low delaying 11 4 44.2 �� 1.8 -222.8 �� 145.3 6.18 �� 0.58 22.9 �� 4.6 *Raven���s data were collected on the imaging subjects only. 2 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1108561108 Casey et al.