Anterior insula reactivity during certain decisions is associated with neuroticism

Abstract

Neuroticism is a core personality trait that profoundly affects how individuals interpret and interact with their environment. Understanding neuroticism at a neurobiological level will be an important step toward identifying novel vulnerability factors for psychiatric illnesses such as depression and anxiety. Along these lines, recent work has identified neural activation patterns within the right anterior insula that correlates with an individual's degree of neuroticism. The present study aims to further characterize the circumstances under which neuroticism modulates insular activity. Sixteen healthy participants underwent functional magnetic resonance imaging while playing a card game with varying degrees of outcome uncertainty. Activation within the bilateral anterior insula was found during all decisions, irrespective of uncertainty. However, a significant positive correlation between neuroticism and anterior insula activity was found only during 'certain decisions' (i.e. situations where the most probable outcome was clearly evident). Moreover, an increase in the right anterior insula activity during certain decisions was related to a behavioral mirroring effect such that the response latency for certain decisions approached the response latency for uncertain decisions. These findings suggest that increasing levels of neuroticism modulate neural activation in such a way that the brain interprets certainty as uncertain.

Fig. 1

The card paradigm. Each trial begins with a 2000 ms presentation of a cue card, during which time the subject (as previously instructed) does not respond. The words ‘Lower’ and ‘Higher’ are then presented at the bottom of the screen, at which point a response can be made. After the selection of a response, all stimuli are removed from the gray background image for a fixed interval of 3500 ms. This delay period is followed by the presentation of a feedback card, along with the message corresponding to the outcome (i.e. ‘You Win’ or ‘You Lose’) and a short sound clip (either a pleasant chime for winning or an aversive buzz for losing). The feedback card remains on the screen for 1500–3500 ms (depending on the subject's latency to select a response). After each trial, a baseline fixation cross is presented for a variable length of time (randomized between 4000–6000 ms). Each trial ranges from 13–15 s in length. Two different subject-specific regressors were created for each trial: (i) the Action Selection regressor begins at the onset of the cue card and ends when the subject selects a response and (ii) the Outcome regressor begins at the onset of the feedback card and ends at the onset of the fixation cross.

Fig. 2

Behavioral results from the fMRI experiment. (A) Each marking represents the subjects’ average probability of predicting the feedback card to be lower than the cue card. The thin black lines represent the SEM. The dashed-line represents the probability of the feedback card actually being lower based on the paradigm's design. (B) To quantify uncertainty, we computed the entropy associated with each cue card. From an information theory perspective, entropy is defined as the degree of uncertainty within a decision as measured by the formula: h = −(p×log₂ p+(1-p)log₂(1−p)), where, ‘p’ represents the fraction of responses where a ‘higher’prediction was selected (Shannon and Weaver, 1949). An entropy of 1 bit reveals a high degree of uncertainty, while an entropy of 0 bit reveals a high degree of certainty. (C) Subjects took significantly longer to select a response during uncertain trials (cue card = 5, 6 or 7) compared with certain trials (cue card = 2, 3, 4, 8, 9 or 10). Response latency is calculated starting from the onset of the ‘Lower/Higher’ prompt (i.e. after the initial 2 s presentation of the cue card). The thin black bars represent the SEM.

Fig. 3

The inset contains a bar graph of the average group activation in the bilateral dLPFC during action selection. Based on this group average, the dLPFC was significantly more active during uncertain trials when compared with certain trials. However, only during certain trials did individual differences in dLPFC reactivity significantly correlate with neuroticism. The scatter plot displays each subject's average activation within the dLPFC during the action selection period of certain trials and his or her respective neuroticism score. There is a significant positive correlation, such that the higher a subject's dLPFC activation, the greater their level of neuroticism.

Fig. 4

The inset contains a bar graph of the average group activation in the bilateral anterior insula during action selection. Based on this group average, the anterior insula was equally active during both certain and uncertain trials. However, only during certain trials did individual differences in anterior insula reactivity significantly correlate with neuroticism. The scatter plot displays each subject's average activation within the anterior insula during the action selection period of certain trials and his or her respective neuroticism score. There is a significant positive correlation, such that the higher a subject's insula activation, the greater their level of neuroticism.

Fig. 5

The scatter plot displays each subject's average activation within the right anterior insula during the action selection period of certain trials and his or her respective response latency difference (in milliseconds) between certain and uncertain trials. There is a significant positive correlation, such that the higher a subject's insula activation, the closer their response latency on certain trials matched their response latency on uncertain trials.