Activity of Frontal and Temporal Circuits in Moments of Real-Life Courage. Highlights; * Courage is associated with dissociation of reported fear and somatic arousal * Subgenual ACC and temporal pole activity correlates positively with courage * Amygdala activity correlates negatively with reported fear when courageous * Subgenual ACC activity correlates positively with reported fear when courageous. Summary; * How does the brain encode courage in a real-life fearful situation that demands an immediate response? In this study, volunteers who fear snakes had to bring a live snake into close proximity with their heads while their brains were scanned using functional magnetic resonance imaging (fMRI). Bringing the snake closer was associated with a dissociation between subjective fear and somatic arousal. Activity in the subgenual anterior cingulate cortex (sgACC) and the right temporal pole was positively correlated with such action. Further, activity in the sgACC was positively correlated with the level of fear upon choosing to overcome fear but not upon succumbing to it. Conversely, activity in a set of interrelated temporal lobe structures, including the amygdala, was attenuated as the level of fear increased when choosing to overcome fear. We propose how the internally reinforced fast representational shift, in which the courageous-response representation gains control over behavior, takes place. The Roman philosopher Seneca
considered all humans slaves to fear (Seneca, 1969). Yet given the right circumstances, ordinary people can set themselves free of this bondage and act courageously. How is this achieved? To act courageously may mean in ordinary discourse anything from rescuing a child from turbulent waters to selecting a risky academic career. Such a broad spectrum of behaviors hence spans different situations and time intervals. However, the wide spectrum of courageous behaviors does have a common denominator, which is the performance of voluntary action opposed to that promoted by ongoing fear (Rachman, 1984,Rachman, 1990,Rachman, 2004a). This suggests that rather different manifestations of courage might share some core brain mechanisms. It is noteworthy that courage as here conceived focuses on action (in spite of fearfulness) that is observed in the general population rather than on an exceptional trait (fearlessness). Thus, by gauging properly defined actions of either overcoming fear or succumbing to it in an acute controllable fearful situation, one can render certain neural substrates of courage amenable to investigation in a brain research laboratory setting. Because it has to do with action to overcome fear, the study of brain mechanisms of courage is expected to overlap with the prolific research on brain mechanisms of fear (LeDoux, 1996), fear extinction (Quirk et al., 2006), and cognitive control of emotion (Ochsner and Gross, 2005). There are, however, notable differences. Experimental extinction deals with gradual reconditioning to appreciate that a conditioned fear response is not warranted any more because the original source of fear has vanished, whereas courageous action as considered here involves prompt voluntary overcoming of the fear reaction to an acute,
on-line source of fear. And although courage clearly involves emotion control, in research protocols of cognitive control of emotion, participants are commonly instructed to use specific cognitive strategies to regulate emotion, while success or failure of this regulation is not instrumental in generating a behavioral outcome, nor does it affect the unfolding of the experimental protocol. In contrast, real-life courage involves uninstructed idiosyncratic regulation strategies leading to behavioral outcomes that in turn influence future decisions and actions. To the best of our knowledge, to date, no functional brain imaging studies have been reported that allow a choice between succumbing to a naturalistic source of fear or overcoming it and acting on the choice; hence, there are none that have probed brain mechanisms of swift decision and action to overcome ongoing fear. In this study we devised a paradigm that enables induction of a sustained acute ecological fear ambience within a functional magnetic resonance imaging (fMRI) scanner, while allowing participants instant choices between overcoming and succumbing to the ongoing fear and a behavioral expression of these choices. We selected a snake as the fear-eliciting stimulus because fear of snakes, often intense, is common in the general population (Agras et al., 1969). Specifically, a live snake (corn snake, Elaphe guttata, ∼1.5 m long) or a toy bear (a control stimulus intended to evoke no fear) were secured to the top of a trolley that could travel step-wise on a conveyer belt spanning the distance between the far end of the scan room and close proximity to the participant’s head within the scanner. Participants were instructed that their task was to reach maximal proximity to the objects, while overcoming to the best of their ability the fear they
might experience. In each trial, the participants were prompted to choose whether to move the object one step closer (Advance) or further away (Retreat) by pressing a response button while their brains were scanned using fMRI (Figure 1). During scanning, the subjective fear rating and skin conductance response (SCR) for each decision were recorded as well. The participants were also evaluated for trait anxiety in general and for state anxiety in the experiment. Two groups of volunteers took part in the study, selected to permit multiple intra- and intergroup analyses of behavioral performance, physiological reaction, and brain activity: Fearful, composed of healthy individuals who fear snakes and who were selected by using a validated snake anxiety questionnaire (SNAQ, Klorman et al., 1974), and Fearless, composed of individuals accustomed to handling snakes. In the following, we describe behavioral, physiological, and brain correlates of the task. By combining our findings with current models of fear regulation, we propose a model of brain mechanisms that could account for what we observe when individuals are engaged in moments of real-life courage. Figure 1 The Experimental Setup and Protocol (A) The participants’ task was to reach maximal proximity to either a live snake (Snake) or a toy bear (Toy Bear), by repeatedly choosing whether to bring the object closer (Advance) or move it away (Retreat), while undergoing fMRI brain scanning. (B) Each trial began with a black screen occluding the participant’s view (Black screen), after which it was lowered (Expose Object) to allow full view of the object on the trolley. Following removal of the screen a brief delay was enforced (Delay), after which the word “Choose” was sounded via earphones. The participant then expressed the choice (Advance or Retreat) by pressing
one of two response device buttons (Choice). The time between beginning of exposure of the object and the choice button press was defined as the choice event of interest (denoted in red). Following the choice the black screen was raised (Conceal Object) to again occlude the participant’s view (Black screen). Next, the black screen was lowered so as to expose only a Visual Analog Scale (VAS) display (Expose VAS) and the participant heard the word “Rate.” The participant then indicated the fear level felt during the last choice by using the response device (Rating), after which the VAS curser changed color (VAS feedback) to indicate that the rating had been recorded. The black screen was then again raised (Conceal VAS) to completely block the participant’s view, after which occured the concealed movement of the trolley according to the last choice. If no choice was made within the set time limit, the trolley retreated. The trials were repeated until the trolley reached maximal proximity to the participant or until a minimum of 20 Advance and 20 Retreat (or no choice) selections were made. (C) Illustrative behavior of a Fearful (FF) participant, depicting the position of the object (Snake, Toy Bear) relative to the participant (starting from 0, most distant from the participant, to 25 (maximum) or less, nearest to the participant), at all consecutive choices made by the participant. Thus, each decent of the line in the graph signifies a retreat choice and each ascent an approach choice. The first 15 choices in the Snake condition made by this participant were Advance after which Retreat and Advance choices were made intermittently. news from: news from: cell.com/neuron
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