Somatic responses in behavioral inhibition

PAUL WHITNEY 0 JOHN M. HINSON 0 AARON WIRICK 0 HEATHER HOLBEN 0 0 Washington State University , Pullman, Washington In the present study, skin conductance responses (SCRs) were measured postdecision and prefeedback in a go/no-go (GNG) task in which participants used response feedback to learn when to respond or not to respond to numeric stimuli. Like somatic markers in gambling tasks and somatic reactions to error monitoring in choice reaction time tasks, SCR patterns distinguished between correct and incorrect trials over time. These somatic reactions were disrupted by a reversal of GNG contingencies, and they were facilitated by pretraining of the stimulus-response mappings. In all cases, however, the somatic reactions appeared to be a product of competent decision making rather than a contributor to performance. Differential somatic responses to good and bad choices appear to be a robust and fairly general phenomenon, but researchers should be cautious in assuming that the somatic responses contribute to performance. - The ability to inhibit responses is an important component of cognitive control and a major focus of study in cognitive neuroscience. Failures of inhibitory control are characteristic of a wide range of neuropsychiatric disorders (see, e.g., Barkley, 1997; Hershey et al., 2004), and in the general population, inhibitory control problems are related to risk for substance abuse and other potentially damaging behavior problems (e.g., Finn, Justus, Mazas, & Steinmetz, 1999; Swann, Bjork, Moeller, & Dougherty, 2002). Research with brain-injured and normal subjects shows that the different tasks used to assess inhibitory control ability share some common processes, but no single mechanism or brain circuit controls all types of inhibition (cf. Hamilton & Martin, 2005; Miyake et al., 2000). Even in the case of relatively simple motor inhibition tasks, there is a long-standing debate concerning whether the inhibition of initial motor activation is exercised by the central executive system or whether it is based on lateral inhibition without central executive control (see Band, Ridderinkhof, & van der Molen, 2003; Gratton, Coles, Sirevaag, Eriksen, & Donchin, 1988; Shimamura, 1995). More recently, both neuroimaging and lesion data have indicated that the supplementary motor area, the dorsolateral prefrontal cortex (DLPFC), the anterior cingulate, and the ventromedial prefrontal cortex (VMPFC) are involved in response inhibition to varying degrees, depending on the response to be inhibited and the complexity of the task (see, e.g., Clark, Cools, & Robbins, 2004; Dias, Robbins, & Roberts, 1997; Mostofsky et al., 2003). One of the most well-validated procedures used in these studies of behavioral inhibition is the go/no-go (GNG) task (e.g., Band et al., 2003; Braver, Barch, Gray, Molfese, & Snyder, 2001). The GNG task requires a rapid decision about whether to respond to a particular stimulus. For example, in a simple version of the GNG task, subjects are instructed to press a key when they see any letter other than X, and to withhold a response to the letter X. Because the letter X appears on only about 20% of trials and the subject must respond rapidly, the prepotent response is to press the key. Problems with behavioral inhibition are assessed by the rate of keypresses to the letter X (i.e., false alarms). Although false alarms in GNG tasks are often considered to be a measure of motor impulsiveness, several different frontal circuits are involved in inhibiting the prepotent responses (e.g., Hershey et al., 2004; Mostofsky et al., 2003). A somewhat more complex version of the GNG task that is relevant to the present research adds a learning component to the requirement of inhibiting a prepotent response (e.g., Finn et al., 1999; Newman & Kosson, 1986). Subjects are presented two-digit numbers as stimuli and must learn which digits are in go and no-go sets on the basis of monetary gains and losses for correct and incorrect decisions. After the subjects learn which stimuli are in the go and no-go sets, the response requirements are reversed without warning so that the go stimuli become no-go stimuli, and vice versa. False alarms, particularly in the reversal phase, are an index of problems with behavioral inhibition. For example, Finn et al. found that alcohol administration increased false alarms in both the initial learning phase and the reversal phase of this GNG task. In the present study, we used this GNG task to investigate somatic responses associated with behavioral inhibition performance. Our aim was to determine whether participants would develop somatic reactions during the learning phase of the GNG task that are analogous to the reactions obtained in more deliberative decision tasks such as the Iowa gambling task (GT) (Bechara, 2004; Bechara, Damasio, Tranel, & Damasio, 1997; Damasio, 1994). On the basis of their research with the GT, Damasio, Bechara, and colleagues have proposed the somatic marker hypothesis, an influential theory of the role of somatic processes in decision making. In the GT, participants begin with a hypothetical stake of money and make choices from decks of cards that can increase or decrease their pool of money. The object of the GT is to make choices that will increase winnings as much as possible. As people make choices, their affective reactions are monitored using skin conductance responses (SCRs). In the most commonly used version of the GT, there are two bad decks that yield some large gains, but with even larger losses, and two good decks that yield smaller short-term gains, but which produce net long-term gains. Over time, the best performers make a higher proportion of choices from the good decks. As people learn to make more choices from the good decks, they also show anticipatory SCRs before making a choice. These SCRs, which Damasio and colleagues conceive of as somatic markers, allow one to distinguish between choices from good and bad decks. The somatic marker hypothesis claims that when a choice is made from alternatives that have each produced gains and losses, the VMPFC is responsible for activating neural circuitry that reconstitutes a somatic state. This somatic state, which can be monitored through SCRs, represents the integration of the previous instances of reward and punishment related to the choice options, and the activated somatic state can unconsciously guide the decision process (Bechara et al., 1997). The most compelling evidence that anticipatory SCRs may reflect a somatic process that facilitates decision making comes from studies of patients with damage to the VMPFC (e.g., Bechara et al., 1997). The VMPFC patients choose more cards from the bad decks, and, unlike normal controls, they do not show anticipatory SCRs to choices from good and bad decks. The somatic marker hypothesis has become quite controversial, in part because of conflicting results over whether performance is determined b (...truncated)