Individual Differences in Impulsivity Predict Anticipatory Eye Movements

Citation: Cirilli L, de Timary P, Lefe`vre P, Missal M ( Individual Differences in Impulsivity Predict Anticipatory Eye Movements Laetitia Cirilli 0 Philippe de Timary 0 Phillipe Lefe` vre 0 Marcus Missal 0 Wael El-Deredy, University of Manchester, United Kingdom 0 1 Institute of Neurosciences (IoNS), Universite Catholique de Louvain , Brussels , Belgium , 2 Department of Adult Psychiatry, Academic Hospital Saint-Luc , Brussels , Belgium , 3 Institute of Information and Communication Technologies, Electronics and Applied Mathematics (ICTEAM), Universite catholique de Louvain , Louvain-la-Neuve , Belgium Impulsivity is the tendency to act without forethought. It is a personality trait commonly used in the diagnosis of many psychiatric diseases. In clinical practice, impulsivity is estimated using written questionnaires. However, answers to questions might be subject to personal biases and misinterpretations. In order to alleviate this problem, eye movements could be used to study differences in decision processes related to impulsivity. Therefore, we investigated correlations between impulsivity scores obtained with a questionnaire in healthy subjects and characteristics of their anticipatory eye movements in a simple smooth pursuit task. Healthy subjects were asked to answer the UPPS questionnaire (Urgency Premeditation Perseverance and Sensation seeking Impulsive Behavior scale), which distinguishes four independent dimensions of impulsivity: Urgency, lack of Premeditation, lack of Perseverance, and Sensation seeking. The same subjects took part in an oculomotor task that consisted of pursuing a target that moved in a predictable direction. This task reliably evoked anticipatory saccades and smooth eye movements. We found that eye movement characteristics such as latency and velocity were significantly correlated with UPPS scores. The specific correlations between distinct UPPS factors and oculomotor anticipation parameters support the validity of the UPPS construct and corroborate neurobiological explanations for impulsivity. We suggest that the oculomotor approach of impulsivity put forth in the present study could help bridge the gap between psychiatry and physiology. - Funding: This work was supported by the Belgian Fonds National de la Recherche Scientifique, the Fondation pour la Recherche Scientifique Medicale, the Belgian Program on Interuniversity Attraction Poles initiated by the Belgian Federal Science Policy Office, and internal research grants from the Universite catholique de Louvain (Fonds Speciaux de Recherche, Action de Recherche Concertee). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Impulsivity describes ones tendency to act without forethought. It is a personality trait that profoundly influences ones behavior and can be an indicator of the development of several psychiatric diseases [1]. To organize behavior and allow some degree of anticipation of future events, the brain needs to make predictions based on information received from sensory organs. From these predictions emerges a representation of how ones action may influence the world [2]. We believe therefore that impulsive actions and abnormal behavior might be due to the inability of individuals to set up predictions normally. A specific example of the brain making predictions based on the repetition of a task is the generation of anticipatory eye movements in response to a moving target. If impulsivity is indeed connected with the basic neurological processes underlying prediction, we expect that it should be correlated with anticipatory eye movements that specifically depend on prediction. Thus, the aim of this paper is to study the relationship between impulsivity and anticipatory eye movements, i.e. saccades and smooth pursuit. The UPPS [3] is a well validated and frequently used questionnaire that distinguishes four independent dimensions of impulsivity: Urgency, lack of Premeditation, lack of Perseverance, and Sensation seeking. The first three dimensions describe deficits related to negative aspects of impulsivity: the difficulty to restrain behavioral reactions in situations that elicit strong emotion (Urgency), the difficulty to anticipate expected situations (lack of Premeditation), and the difficulty to sustain prolonged, enduring activity (lack of Perseverance). The fourth dimension, sensation seeking, is a positive dimension that describes the tendency to search for new, highly emotionally-arousing situations. Besides being strongly related to pathology [1], impulsivity (particularly lack of premeditation) has also been related to deficits in decision making [4] as measured by choice tasks such as the Iowa Gambling task, and even to the depreciation of rewards as measured by delay discounting tasks [5-7]. However, these tasks test slow, complex cognitive processes. So far, the possibility that impulsivity could be related to basic, low level neural mechanisms has never been examined. In this study, we tested the possibility that impulsivity is related to standard oculomotor measures such as the latency and speed of anticipatory eye movements. One dimension of impulsivity in particular, the lack of premeditation, is by definition a difficulty in anticipating future events. We therefore expect that it could be well-correlated with the anticipatory oculomotor measures. Anticipation has often been studied using eye movements as a tool. Indeed, saccadic and smooth anticipatory eye movements have been well described in humans and other primates [821], and the role of frontal structures involved in their control has been partly elucidated [2226]. The interest of testing whether the characteristics of anticipatory movements correlate with UPPS scores is twofold. Firstly, it would help to understand the idiosyncratic differences in oculomotor anticipation between humans. Indeed, it has been often observed that there are large variations between humans in their capacity to initiate anticipatory movements [13]; M. Missal, personal observation). Some human healthy subjects are good anticipators, others are not. Secondly, finding a correlation would relate a personality trait commonly described in psychiatry with a well characterized, objectively measurable behavior, whereas questionnaires on personality may be subject to personal biases. Specific facets of impulsivity could be sustained by the same neurophysiological processes known to modulate anticipatory eye movements, involving the cortical-basal ganglia oculomotor loop. Indeed, the basal ganglia and the dopamine are dysregulated in impulsive subjects [7,2729]. Therefore, observed correlations would suggest that this important personality trait could be related to physiological mechanisms that are responsible for the development of anticipation, i.e. setting up (...truncated)