Sleep Deprivation Alters Valuation Signals in the Ventromedial Prefrontal Cortex in Singapore
Reported, January 4, 2012
Even a single night of total sleep deprivation (SD) can have dramatic effects on economic decision making. Here we tested the novel hypothesis that SD influences economic decisions by altering the valuation process. Using functional magnetic resonance imaging we identified value signals related to the anticipation and the experience of monetary and social rewards (attractive female faces). We then derived decision value signals that were predictive of each participants willingness to exchange money for brief views of attractive faces in an independent market task. Strikingly, SD altered decision value signals in ventromedial prefrontal cortex (VMPFC) in proportion to the corresponding change in economic preferences. These changes in preference were independent of the effects of SD on attention and vigilance. Our results provide novel evidence that signals in VMPFC track the current state of the individual, and thus reflect not static but constructed preferences.
A single night of total sleep deprivation (SD) can result in a host of neurocognitive consequences (Goel et al., 2009). Most comprehensively studied have been impairments in vigilance and attention (Lim and Dinges, 2010). Considerably less is known about how SD influences affective processes (Walker, 2009), for example, those engaged during decision making (Harrison and Horne, 1999; Killgore et al., 2006; McKenna et al., 2007; Venkatraman et al., 2007). Studies to date have evaluated risky decisions using the Iowa Gambling Task (Killgore et al., 2006), risky and ambiguous decision making tasks (McKenna et al., 2007; Venkatraman et al., 2007, 2011), and the Balloon Analog Risk Task (Killgore et al., 2011). Increased propensity to take risks has been observed in some of these studies and an intriguing possibility is that SD affects decision making by influencing the very values that underlie our decisions. Investigating this potential mechanism would benefit from measuring the neural correlates of reward valuation without involving decision making.
Recent studies suggest that decision preferences reflect the subjective valuation of different goods that have been converted into a standard signal, or common neural currency (Montague and Berns, 2002; Izuma et al., 2008; Kim et al., 2010; Rademacher et al., 2010; Smith et al., 2010). This common neural currency enables individuals to make decisions about nominally incommensurable rewards, as when sacrificing a physical or monetary good to obtain a desirable social interaction (Smith et al., 2010; Lin et al., 2011). Such common valuation signals have been demonstrated in ventromedial prefrontal cortex (VMPFC), through correlative techniques such as functional magnetic resonance imaging (fMRI) and single-unit recording (Padoa-Schioppa and Assad, 2006, 2008; Chib et al., 2009; Padoa-Schioppa, 2009; Kim et al., 2010; Smith et al., 2010). One limitation of the extant research is that nearly all studies manipulate value by changing the stimuli about which individuals make decisions (e.g., comparing high- and low-valued items). Yet, in the real-world, our valuation of an outcome depends both on its intrinsic features and on our current state. SD provides an ideal milieu for testing state-dependent changes in valuation: it allows for fully within-participant testing, it has no effects on the actual value of economic goods (unlike presenting food items under states of satiation and hunger), and it represents a common and ecologically relevant state that nearly all individuals experience at some time in their lives.
We hypothesized that SD can alter valuation and perturb the neural common currency for value as reflected by VMPFC activation. This hypothesis stems from the observation that VMPFC activation was altered during risky decision making when sleep deprived (Venkatraman et al., 2011). In turn, these changes in decision value signals would be expected to be commensurate with shifts in valuation of different reward types demonstrating that VMPFC plays an important role in coding a common currency signal. This second prediction stems from observing that SD also affects activation of regions involved in emotional processing (Yoo et al., 2007; Gujar et al., 2011). We used an incentive delay task in which participants anticipated and then received rewards that had either monetary value or social value [e.g., pictures of faces of varying attractiveness . Following the scanner session, we measured each subjects willingness to sacrifice money to view attractive faces (Smith et al., 2010) This procedure was motivated by evidence that signals reflecting subjective value can be elicited by incentive-compatible stimuli even in the absence of overt decision making (Lebreton et al., 2009; Smith et al., 2010; Tusche et al., 2010). The measurement of these brain signals provides a neural marker for subjective value independent of the effects of SD on decision making (Venkatraman et al., 2007). We anticipated that changes in an individuals relative willingness to trade social and monetary rewards following SD would be correlated with a corresponding alteration of neural signals corresponding with their valuation. Such a result would provide evidence that SD affects more than attentional and cognitive inputs to a decision it shapes the very mechanisms of valuation that underlie economic preferences.
Twenty-two healthy adult males (mean age=22.7years, SD=3.2years), self-reported as heterosexual, participated in the study. All participants provided informed consent, in compliance with the requirements of the National University of Singapore Institutional Review Board. Participants were selected from a pool of university students who responded to a web-based questionnaire. They had to be right-handed, be between 18 and 30years of age, not be on any long-term medication, and have no history of any psychiatric or neurologic disorders. They also had to have habitually good sleeping habits (sleeping no less than 6.5h each night for the past 1month) and have no symptoms associated with sleep disorders. Participants sleep habits were monitored throughout the 2-week duration of the study with an Actiwatch (Philips Respironics, USA). Only participants who maintained a regular sleep schedule (>6.5h of sleep/night; sleep time no later than 1:00 AM; wake time no later than 9:00 AM) for the week prior to each fMRI scanning session were included in the study. Four participants were removed from the analysis: one for excessive motion during the scan, and three for failure to perform the task appropriately during the SD session. All participants indicated that they did not smoke, consume any medications, stimulants, caffeine, or alcohol for at least 24h prior to scanning.
The reward value of an item influences the effort expended in acquiring it (Bickel et al., 1992; Aharon et al., 2001). In the Incentive Delay Task (see Materials and Methods), increasing effort is reflected in shorter response times. Three factors were expected to influence response times: behavioral state (SD or RW), reward modality (social or money), and reward magnitude (high, medium, low).
Consistent with prior work, a three-way ANOVA showed a significant interaction between reward type and reward magnitude [F(3,54)=35.18, p<0.001]. A two-way ANOVA of reaction time for monetary rewards showed significant main effects of reward magnitude [F(2,17)=23.07, p<0.001] and state [F(1,17)=6.61), p<0.05] on response time but no interaction between these factors [F(2,17)=2, n.s.]. Similarly, for social rewards there were significant main effects of reward magnitude [F(2,17)=10.89, p<0.001] and state [F(1,17)=8.65, p<0.01] on response times without significant interaction between reward and state [F(2,17)=0.27, n.s.]. These findings formed the behavioral basis for the identification of brain regions involved in the valuation of monetary and social rewards.
The relative valuation of social and monetary rewards was ascertained by analyzing decisions in the Exchange Task. Following a normal night of sleep (RW), participants ranged from being unwilling to exchange money to view an attractive face, to exchanging in over 90% of the trials. Although the average exchange rate did not differ across the two sessions the mean exchange rate being 24.9% in RW and 24.0% in SD [t(17)=0.62, n.s.] individual participants showed a range of alterations in willingness to exchange money to view attractive faces, with some participants exchanging more and some exchanging less following SD.
The heterogeneous alteration in exchange behavior following SD may be the result of random fluctuation in choices rather than a systematic alteration of preferences. To rule out this possibility, we examined the consistency of exchange rates across runs within the same session. Within-session exchange rates were similarly consistent across both states (ICC of 0.939 for RW and 0.936 for SD), arguing against increased randomness in choices following SD. As a control experiment, we recruited an additional independent group of participants to perform the exchange task twice in RW. Consistent with the expectation that SD was the source of altered exchange behavior, we found the variance associated with RWSD exchanges to be larger than the variance associated with RWRW exchanges (Levene test, F=4.58, p<0.05,). Finally, order of sessions could not explain the shifts in exchange rate [t(17)=-1.56, n.s.].
To ascertain whether SD prompted alteration in exchange behavior by shifting the perceived (social) value of attractive faces, we had subjects rate faces for attractiveness in both states. We found strong correlation between the state-driven alteration in exchange rates between RW and SD and the corresponding difference in attractiveness ratings (r=0.84, p<0.001;).
Finally, if participants altered their valuation of social, but not monetary, rewards in a consistent manner during SD, we would expect this to be reflected in the reaction times during the Incentive Delay Task. Indeed, the SD-induced change in exchange rate was significantly correlated with a corresponding change in reaction time for the higher levels of social reward 5-star and 3-star faces (r=0.48; p<0.05) but not for control cues, 1-star faces, or monetary rewards (r<0.26; n.s.,). Taken together, these behavioral findings suggest that the shift in exchange rates elicited by SD were a consequence of altered valuation of social as opposed to monetary rewards.
Additionally, altered psychomotor vigilance (Dinges et al., 1997), as evidenced by increased RT during SD [RW: 242ms, SD: 291ms; t(17)=6.5, p<0.001], did not correlate with alteration of exchange behavior (r=-0.04; n.s.). This result concurs with a prior finding that vigilance and the propensity to make gain-maximizing decisions are uncorrelated (Venkatraman et al., 2011).
We have shown that the VMPFC, a region that integrates valuation signals for different rewards into a common scale, demonstrates a shift in activation commensurate with shift in behavior across states. This strengthens the notion that VMPFC is involved in value comparisons during economic decision making independent of state. Additionally, regions involved in social reward valuation, such as the amygdala, alter their responses to social rewards during SD in a manner that is correlated with the shift in decision value signals in VMPFC. This suggests that the changes in VMPFC activation could be the result of state-related alteration of inputs from the amygdala and other regions mediating affective processes.
Credits:Camilo Libedinsky,David V. Smith,Chieh Schen Teng,Praneeth Namburi,Vanessa W. Chen,Scott A. Huettel,and Michael W. L. Chee
More Information at:
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3199544/?tool=pubmed