Effects of Pulvinar Inactivation on Spatial Decision-making between Equal and Asymmetric Reward Options

The ability to selectively process visual inputs and to decide between multiple movement options in an adaptive manner is critical for survival. Such decisions are known to be influenced by factors such as reward expectation and visual saliency. The dorsal pulvinar connects to a multitude of cortical areas that are involved in visuospatial memory and integrate information about upcoming eye movements with expected reward values. However, it is unclear whether the dorsal pulvinar is critically involved in spatial memory and reward-based oculomotor decision behavior. To examine this, we reversibly inactivated the dorsal portion of the pulvinar while monkeys performed a delayed memory saccade task that included choices between equally or unequally rewarded options. Pulvinar inactivation resulted in a delay of saccade initiation toward memorized contralesional targets but did not affect spatial memory. Furthermore, pulvinar inactivation caused a pronounced choice bias toward the ipsilesional hemifield when the reward value in the two hemifields was equal. However, this choice bias could be alleviated by placing a high reward target into the contralesional hemifield. The bias was less affected by the manipulation of relative visual saliency between the two competing targets. These results suggest that the dorsal pulvinar is involved in determining the behavioral desirability of movement goals while being less critical for spatial memory and reward processing

Effects of Pulvinar Inactivation on Spatial Decision-making between Equal and Asymmetric Reward Options

The ability to selectively process visual inputs and to decide between multiple movement options in an adaptive manner is critical for survival. Such decisions are known to be influenced by factors such as reward expectation and visual saliency. The dorsal pulvinar connects to a multitude of cortical areas that are involved in visuospatial memory and integrate information about upcoming eye movements with expected reward values. However, it is unclear whether the dorsal pulvinar is critically involved in spatial memory and reward-based oculomotor decision behavior. To examine this, we reversibly inactivated the dorsal portion of the pulvinar while monkeys performed a delayed memory saccade task that included choices between equally or unequally rewarded options. Pulvinar inactivation resulted in a delay of saccade initiation toward memorized contralesional targets but did not affect spatial memory. Furthermore, pulvinar inactivation caused a pronounced choice bias toward the ipsilesional hemifield when the reward value in the two hemifields was equal. However, this choice bias could be alleviated by placing a high reward target into the contralesional hemifield. The bias was less affected by the manipulation of relative visual saliency between the two competing targets. These results suggest that the dorsal pulvinar is involved in determining the behavioral desirability of movement goals while being less critical for spatial memory and reward processing

Inactivation of Parietal Reach Region Affects Reaching But Not Saccade Choices in Internally Guided Decisions

The posterior parietal cortex (PPC) has traditionally been considered important for awareness, spatial perception, and attention. However, recent findings provide evidence that the PPC also encodes information important for making decisions. These findings have initiated a running argument of whether the PPC is critically involved in decision making. To examine this issue, we reversibly inactivated the parietal reach region (PRR), the area of the PPC that is specialized for reaching movements, while two monkeys performed a memory-guided reaching or saccade task. The task included choices between two equally rewarded targets presented simultaneously in opposite visual fields. Free-choice trials were interleaved with instructed trials, in which a single cue presented in the peripheral visual field defined the reach and saccade target unequivocally. We found that PRR inactivation led to a strong reduction of contralesional choices, but only for reaches. On the other hand, saccade choices were not affected by PRR inactivation. Importantly, reaching and saccade movements to single instructed targets remained largely intact. These results cannot be explained as an effector-nonspecific deficit in spatial attention or awareness, since the temporary “lesion” had an impact only on reach choices. Hence, the PPR is a part of a network for reach decisions and not just reach planning

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

Dynamic Integration of Value Information into a Common Probability Currency as a Theory for Flexible Decision Making

Decisions involve two fundamental problems, selecting goals and generating actions to pursue those goals. While simple decisions involve choosing a goal and pursuing it, humans evolved to survive in hostile dynamic environments where goal availability and value can change with time and previous actions, entangling goal decisions with action selection. Recent studies suggest the brain generates concurrent action-plans for competing goals, using online information to bias the competition until a single goal is pursued. This creates a challenging problem of integrating information across diverse types, including both the dynamic value of the goal and the costs of action. We model the computations underlying dynamic decision-making with disparate value types, using the probability of getting the highest pay-off with the least effort as a common currency that supports goal competition. This framework predicts many aspects of decision behavior that 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

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