Neural activity in the human brain relating to uncertainty and arousal during anticipation

Abstract

with ventromedial prefrontal lesions select the high-risk 12 Queen Square strategy (Bechara et al., 1996). In contrast, intact sub-Institute of Neurology jects adopt the more advantageous low-risk strategy University College London with learning (Bechara et al., 1997, 1999). With learn-London WC1N 3BG ing, normal subjects develop anticipatory sympathetic United Kingdom arousal before selecting high-risk options; this anticipa-† Autonomic Unit tory arousal is absent in patients with ventromedial pre-National Hospital for Neurology and Neurosurgery frontal damage, who are indifferent to risk despite nor-London WC1N 3BG mal autonomic responses to such "physical" stimuli as United Kingdom loud noises (Bechara et al., 1996; Tranel, 2000). These ‡ Neurovascular Medicine Unit patients have reduced arousal responses (indexed by St. Mary's Hospital galvanic skin conductance responses [GSR]) to other Imperial College School of Medicine "psychological" stimuli (e.g., affective pictures) (Tranel London W2 1NY and Damasio, 1994; Bechara et al., 1999; Tranel, 2000). United Kingdom The observation of a conjunction between absent anticipatory arousal and maladaptive behavioral strategies has led to a hypothesis that cerebral representation of Summary anticipatory arousal biases behavior and guides strategic decision-making (Damasio et al., 1991; Damasio, We used functional magnetic resonance neuroimag-1994; Bechara et al., 1996). This behavioral bias may be ing to measure brain activity during delay between dissociated from explicit, conscious knowledge about reward-related decisions and their outcomes, and the risk. Healthy subjects show a preference for low-risk modulation of this delay activity by uncertainty and decisions and show increased amplitude of anticipatory arousal. Feedback, indicating financial gain or loss, skin-conductance responses to high-risk options before was given following a fixed delay. Anticipatory arousal developing explicit awareness of the most advantawas indexed by galvanic skin conductance. Delaygeous behavioral strategy (Bechara et al., 1997). Moreperiod activity was associated with bilateral activation over, patients with ventromedial prefrontal cortical lein orbital and medial prefrontal, temporal, and right sions may demonstrate explicit awareness of the risks parietal cortices. During delay, activity in anterior cinassociated with particular decisions but are unable to gulate and orbitofrontal cortices was modulated by modify their behavior accordingly (Saver and Damasio, outcome uncertainty, whereas anterior cingulate, dor-1991; Bechara et al., 1997). Thus, anticipatory arousal is solateral prefrontal, and parietal cortices activity was an index of implicit risk-related learning that may directly modulated by degree of anticipatory arousal. A distinct influence behavior. region of anterior cingulate was commonly activated We used functional magnetic resonance (fMRI) to by both uncertainty and arousal. Our findings highlight measure brain activity in healthy subjects performing a distinct cont...

Predicting events of varying probability: uncertainty investigated by fMRI

“…In addition to posterior frontomedian areas, orbitofrontal areas are known to be engaged in uncertain decisions, particularly those induced by reward expectancy, and depending on varying task-corresponding emotional attitudes (O'Doherty et al, 2001;Rogers et al, 1999;Critchley et al, 2001;Breiter et al, 2001;Elliott et al, 1999). However, due to technical restrictions of the T2* sequence in a 3T NMR system that usually causes signal voids (Norris et al, 2002), medial orbitofrontal activations could not be detected in the present study.…”

“…This difference may include also emotional processes, which should have higher impact on fast behavioral adaptations rather than on long-lasting learning. Accordingly, BA 24/32 is suggested in the integration of cognitive processing of uncertainty with corresponding adaptive changes in bodily states (Critchley et al, 2001) or evaluative processes related to the emotional consequences of a (risky) choice (Elliott and Dolan, 1998).…”

“…Using a parametric design, we tested the hypothesis of whether brain activation within the region of interest, i.e., frontomedian areas, would increase with decreasing event probability. Many different tasks that require decisions or overt responses under uncertainty are known to draw on frontomedian areas (Bechara et al, 1996;Elliott et al, 1999;Elliott and Dolan, 1998;Paulus et al, 2001Paulus et al, , 2002Critchley et al, 2001, Rogers et al, 1999Goel and Dolan, 2000). However, uncertainty is reported to be reflected within posterior frontomedian areas, including mesial BA 8 or anterior BA 6, corresponding to the presupplementary motor area (pre-SMA), and BA 24/32, i.e., the anterior cingulate cortex (ACC).…”

Nonlinear neurobiological probability weighting functions for aversive outcomes

“…One possible reason is that the activation we measured represented a passive response in the absence of a decision. The ACC is a prime candidate for the integration of magnitude and probability information -even in the absence of a required response, because of its prominent integrative role between the affective system and the motor response system (Botvinick et al, 2001;Critchley et al, 2001;Miller and Cohen, 2001). Although prospect theory assumes functional separability of probability and utility functions, the multiplication of these two dimensions must occur somewhere.…”

Three studies on the neuroeconomics of decision-making when payoffs are real and negative

“…One possible reason is that the activation we measured represented a passive response in the absence of a decision. The ACC is a prime candidate for the integration of magnitude and probability information -even in the absence of a required response, because of its role in integrating the affective system and the motor response system (Botvinick, Braver, Barch, Cohen, & Carter, 2001;Critchley, Mathias, & Dolan, 2001;Miller & Cohen, 2001). Although prospect theory assumes functional separability of probability and utility functions, the multiplication of these two dimensions must occur somewhere.…”