A Biologically Plausible Computational Theory for Value Integration and Action Selection in Decisions with Competing Alternatives

Decision making is a vital component of human and animal behavior that involves selecting between alternative options and generating actions to implement the choices. Although decisions can be as simple as choosing a goal and then pursuing it, humans and animals usually have to make decisions in dynamic environments where the value and the availability of an option change unpredictably with time and previous actions. A predator chasing multiple prey exemplifies how goals can dynamically change and compete during ongoing actions. Classical psychological theories posit that decision making takes place within frontal areas and is a separate process from perception and action. However, recent findings argue for additional mechanisms and suggest the decisions between actions often emerge through a continuous competition within the same brain regions that plan and guide action execution. According to these findings, the sensorimotor system generates concurrent action-plans for competing goals and uses online information to bias the competition until a single goal is pursued. This information is diverse, relating to both the dynamic value of the goal and the cost of acting, creating a challenging problem in integrating information across these diverse variables in real time. We introduce a computational framework for dynamically integrating value information from disparate sources in decision tasks with competing actions. We evaluated the framework in a series of oculomotor and reaching decision tasks and found that it captures many features of choice/motor behavior, as well as its neural underpinnings that previously have eluded a common explanation

Lateral intraparietal area (LIP) is largely effector-specific in free-choice decisions

Despite many years of intense research, there is no strong consensus about the role of the lateral intraparietal area (LIP) in decision making. One view of LIP function is that it guides spatial attention, providing a “saliency map” of the external world. If this were the case, it would contribute to target selection regardless of which action would be performed to implement the choice. On the other hand, LIP inactivation has been shown to influence spatial selection and oculomotor metrics in free-choice decisions, which are made using eye movements, arguing that it contributes to saccade decisions. To dissociate between a more general attention role and a more effector specific saccade role, we reversibly inactivated LIP while non-human primates freely selected between two targets, presented in the two hemifields, with either saccades or reaches. Unilateral LIP inactivation induced a strong choice bias to ipsilesional targets when decisions were made with saccades. Interestingly, the inactivation also caused a reduction of contralesional choices when decisions were made with reaches, albeit the effect was less pronounced. These findings suggest that LIP is part of a network for making oculomotor decisions and is largely effector-specific in free-choice decisions

L'influence des oscillations en delta sur la sélection d'une action

Résumé : La capacité de décider parmi plusieurs possibilités d'actions, grâce à l'information sensorielle disponible, est essentielle à un organisme interagissant avec un environnement complexe. Les modèles actuels de sélection d'une action soutiennent que le cerveau traite continuellement l'information sensorielle afin de planifier plusieurs possibilités d'action en parallèle. Dans cette perspective, ces représentations motrices, associées à chaque possibilité d'action, sont en constante compétition entre elles. Afin qu'une alternative puisse être sélectionnée pour le mouvement, une valeur de pondération, intégrant une multitude de facteurs, doit être associée à chacun des plans moteurs afin de venir moduler la compétition. Plusieurs études se sont intéressées aux différents facteurs modulant la sélection de l'action, tels que la disposition de l'environnement, le coût des actions, le niveau de récompense, etc. Par contre, il semble qu'aucune étude n'ait rapporté ce qu'il advient lorsque la valeur de pondération de chacune des actions possibles est identique. Dans ce contexte, quel est l'élément permettant de venir moduler la sélection de l'action? De ce fait, l'objectif principal de mon projet de maitrise est d'investiguer le facteur permettant au cerveau de sélectionner une action lorsque tous les facteurs rapportés dans la littérature sont contrôlés. De récentes données ont montré que les oscillations corticales lentes dans la bande delta peuvent servir d'instrument de sélection attentionnelle en modulant l'amplitude de la réponse neuronale. Ainsi, les stimuli arrivant dans le cortex pendant une phase en delta de forte excitabilité sont amplifiés, tandis que ceux arrivant lors d'une phase en delta de faible excitabilité sont atténués. Ceci dit, il est possible que la phase en delta dans laquelle se trouve le cerveau au moment d'effectuer la sélection d'une action puisse influencer la décision. Utilisant une tâche de sélection de main, cette étude teste l'hypothèse que la sélection de la main est associée à la phase en delta des ensembles neuronaux codant le mouvement de chacune des mains, lorsque tous les facteurs connus influençant la décision sont contrôlés. L'électroencéphalographie (EEG) fut utilisée afin d'enregistrer les signaux corticaux pendant que les participants effectuaient une tâche de sélection de main dans laquelle ils devaient, à chaque essai, atteindre une cible visuelle aussi rapidement que possible en utilisant la main de leur choix. La tâche fut conçue de façon à ce que les facteurs spatiaux et biomécaniques soient contrôlés. Ceci fut réalisé enidentifiant premièrement, sur une base individuelle, l'emplacement de la cible pour laquelle les mains droite et gauche avaient une probabilité équivalente d'être choisies (point d'égalité subjective, PSE). Ensuite, dans l'expérience principale, les participants effectuaient plusieurs mouvements d'atteinte vers des cibles positionnées près et loin du PSE, toujours avec la main de leur choix. L'utilisation de cinq cibles très près du PSE a permis de collecter de nombreux essais dans lesquels la main droite et la main gauche furent sélectionnées en réponse à un même stimulus visuel. Ceci a ainsi permis d'analyser les signaux des deux cortex dans des conditions d'utilisation de la main droite et gauche, tout en contrôlant pour les autres facteurs pouvant moduler la sélection de la main. Les résultats de cette recherche révèlent que l'hémisphère cortical se trouvant dans la phase la plus excitable en delta (près du pic négatif), lors de l'apparition du stimulus, est associé à la fois à la main qui sera sélectionnée ainsi qu'au temps de réaction. Ces résultats montrent que l'excitabilité corticale momentanée (phase du signal) pourrait agir comme un facteur modulant la sélection d'une action. Dans cette optique, ces données élargissent considérablement les modèles actuels en montrant que la sélection d'une action est en partie déterminée par l'état du cerveau au moment d'effectuer un choix, d'une manière qui est indépendante de toutes les variables de décision connues.Abstract : Action selection is thought to be achieved by competitive interactions between simultaneously co-existing motor representations associated with each potential action. Critically, selection via competition requires biasing signals to enable only one of these alternatives to be selected. Here we use electroencephalography in a unique hand selection task in which all decision variables are controlled, and show that the cortical hemisphere that is in the most excitable phase of delta frequency band at target onset dictates the hand to be selected as well as reaction time. These results demonstrate that the momentary excitability of neuronal ensembles in which motor representations are encoded can bias action selection

Lateral intraparietal area (LIP) is largely effector-specific in free-choice decisions

Despite many years of intense research, there is no strong consensus about the role of the lateral intraparietal area (LIP) in decision making. One view of LIP function is that it guides spatial attention, providing a “saliency map” of the external world. If this were the case, it would contribute to target selection regardless of which action would be performed to implement the choice. On the other hand, LIP inactivation has been shown to influence spatial selection and oculomotor metrics in free-choice decisions, which are made using eye movements, arguing that it contributes to saccade decisions. To dissociate between a more general attention role and a more effector specific saccade role, we reversibly inactivated LIP while non-human primates freely selected between two targets, presented in the two hemifields, with either saccades or reaches. Unilateral LIP inactivation induced a strong choice bias to ipsilesional targets when decisions were made with saccades. Interestingly, the inactivation also caused a reduction of contralesional choices when decisions were made with reaches, albeit the effect was less pronounced. These findings suggest that LIP is part of a network for making oculomotor decisions and is largely effector-specific in free-choice decisions

Changes of Mind in voluntary action – Flexibility vs. stability of intentions

Changes of Mind’ can provide insights into the dynamic and continuous processes underlying decision making and action selection. Previous studies on Changes of Mind have exclusively focused on either perceptual or value-based choice. This thesis investigates the flexible neurocognitive mechanisms that shape voluntary actions, which require integration of internally-generated (endogenous) intentions and externally-cued (exogenous) sensory or value-based information. When information is noisy or changes dynamically, agents sometimes change their voluntary intentions and/or change the movements that are required to implement intentions into action. Continuous movement trajectories were used to capture both types of Change of Mind during ongoing action execution, revealing that ‘Changes of Intention’ are more frequent when intentions are weak or when the cost of pursuing an intention is high. These findings could be qualitatively reproduced by an attractor network model that continuously integrates endogenous and exogenous information over time, occasionally switching from one attractor state to a different one later on. In an fMRI study, the neural dynamics of intention reversals were investigated, providing evidence that neural patterns in a fronto-parietal network change dynamically to incorporate new decision- and action-relevant evidence after action onset. Finally, while behavioural flexibility is advantageous in many situations, an important hallmark of voluntary control is intention pursuit despite external changes or challenges. For example, people often need to persevere in the face of effort. Patients with post-stroke fatigue showed reduced perseverance compared to healthy controls when goal pursuit required continuous effort, which may cause adverse health-related outcomes. In conclusion, this thesis provides new insights into the continuous neurocognitive mechanisms that shape voluntary actions as they unfold. Reversibility of intentions allows agents to adjust their own actions to the current context, while stability of intentions is necessary for successful goal pursuit. Hence, volition requires balanced integration of endogenous intentions with dynamically-changing exogenous information