Nonhuman primates exploit the prior assumption that the visual world is vertical.

When human subjects tilt their heads in dark surroundings, the noisiness of vestibular information impedes precise reports on objects' orientation with respect to Earth's vertical axis. This difficulty is mitigated if a vertical visual background is available. Tilted visual backgrounds induce feelings of head tilt in subjects who are in fact upright. This is often explained as a result of the brain resorting to the prior assumption that natural visual backgrounds are vertical. Here, we tested whether monkeys show comparable perceptual mechanisms. To this end we trained two monkeys to align a visual arrow to a vertical reference line that had variable luminance across trials, while including a large, clearly visible background square whose orientation changed from trial to trial. On ∼20% of all trials, the vertical reference line was left out to measure the subjective visual vertical (SVV). When the frame was upright, the monkeys' SVV was aligned with the gravitational vertical. In accordance with the perceptual reports of humans, however, when the frame was tilted it induced an illusion of head tilt as indicated by a bias in SVV toward the frame orientation. Thus all primates exploit the prior assumption that the visual world is vertical.NEW & NOTEWORTHY Here we show that the principles that characterize the human perception of the vertical are shared by another old world primate species, the rhesus monkey, suggesting phylogenetic continuity. In both species the integration of visual and vestibular information on the orientation of the head relative to the world is similarly constrained by the prior assumption that the visual world is vertical in the sense of having an orientation that is congruent with the gravity vector.

A Reinforcement Meta-Learning framework of executive function and information demand.

Gathering information is crucial for maximizing fitness, but requires diverting resources from searching directly for primary rewards to actively exploring the environment. Optimal decision-making thus maximizes information while reducing effort costs, but little is known about the neuro-computational implementation of this tradeoff. We present a Reinforcement Meta-Learning (RML) computational model that solves the trade-off between the value and costs of gathering information. We implement the RML in a biologically plausible architecture that links catecholaminergic neuromodulators, the medial prefrontal cortex and topographically organized visual maps and show that it accounts for neural and behavioral findings on information demand motivated by instrumental incentives and intrinsic utility. Moreover, the utility function used by the RML, encoded by dopamine, is an approximation of variational free energy. Thus, the RML presents a biologically plausible mechanism for coordinating motivational, executive and sensory systems generate visual information gathering policies that minimize free energy.

Uncertainty modulates visual maps during noninstrumental information demand.

Animals are intrinsically motivated to obtain information independently of instrumental incentives. This motivation depends on two factors: a desire to resolve uncertainty by gathering accurate information and a desire to obtain positively-valenced observations, which predict favorable rather than unfavorable outcomes. To understand the neural mechanisms, we recorded parietal cortical activity implicated in prioritizing stimuli for spatial attention and gaze, in a task in which monkeys were free (but not trained) to obtain information about probabilistic non-contingent rewards. We show that valence and uncertainty independently modulated parietal neuronal activity, and uncertainty but not reward-related enhancement consistently correlated with behavioral sensitivity. The findings suggest uncertainty-driven and valence-driven information demand depend on partially distinct pathways, with the former being consistently related to parietal responses and the latter depending on additional mechanisms implemented in downstream structures.

Economic choice between remifentanil and food in squirrel monkeys.

Traditional approaches for evaluating if compounds are reinforcing, and thus a risk for abuse, include preclinical self-administration procedures conducted in the absence of alternative reinforcers. While the track record of this approach for determining abuse potential is good, that for predicting efficacy of addiction treatments is not. An alternate approach would be economic choice between drug and nondrug rewards, with parametrically varied options from trial to trial. This would promote goal-directed decisions between reward modalities and should provide metrics that reflect changes in internal state that influence desirability of a given option. We report herein a high throughput economic choice procedure in which squirrel monkeys choose between a short-lived opiate, remifentanil, and a palatable food reward. Stimuli on touchscreens indicate the amount of each reward type offered by varying the number of reward-specific elements. The rapid clearance of remifentanil avoids accumulation of confounding levels of drug, and permits a large number of trials with a wide range of offers of each reward modality. The use of a single metric encompassing multiple values of each reward type within a session enables estimation of indifference values using logistic regression. This indifference value is sensitive to reward devaluation within each reward domain, and is therefore a useful metric for determining shifts in reward preference, as shown with satiation and pharmacological treatment approaches.

Deliberative Decision-Making in Macaques Removes Reward-Driven Response Vigor.

Most of our daily decisions are governed by one of two systems: an impulsive system driving instantaneous decisions and a deliberative system driving thoughtful ones. The impulsive system reacts to immediately available concrete rewards. In contrast, the deliberative system reacts to more delayed rewards and/or punishments, which imposes consideration of longer-term choice consequences. Contingency management for addiction treatment is hypothesized to engage deliberative processes. Ultimately, in both decision-making situations, an action is needed to enact the decision. Whether those actions differ in implementation is an open question whose answer could inform as to whether distinct neural systems are engaged. To explore whether there is evidence of separate mechanisms between deliberated and immediate choices, we trained monkeys to perform a decision-making task where they made a choice on a touch screen between two visual cues predicting different amounts of reward. In immediate choice (IC) trials, the cues appeared at the final response locations where subjects could immediately touch the chosen cue. In deliberated choice (DC) trials, compound cues appeared orthogonally to the response locations. After a delay, allowing for decision formation, an identifying cue component was displaced to the randomly assigned response locations, permitting subjects to reach for the chosen cue. Both trial types showed an effect of cue value on cue selection time. However, only IC trials showed an effect of the competing cue on response vigor (measured by movement duration) and a reach trajectory that deviated in the direction of the competing cue, suggesting a decision reexamination process. Reward modulation of response vigor implicates dopaminergic mechanisms. In DC trials, reach trajectories revealed a commitment to the chosen choice target, and reach vigor was not modulated by the value of the competing cue. Our results suggest that choice-action dynamics are shaped by competing offers only during instantaneous, impulsive choice. After a deliberated decision, choice-action dynamics are unaffected by the alternative offer cue, demonstrating a commitment to the choice. The potential relevance to contingency management is discussed.

Parietal neurons encode information sampling based on decision uncertainty.

During natural behavior, animals actively gather information that is relevant for learning or actions; however, the mechanisms of active sampling are rarely investigated. We tested parietal neurons involved in oculomotor control in a task in which monkeys made saccades to gather visual information relevant to a subsequent action. We show that the neurons encode, before the saccade, the information gain (reduction in decision uncertainty) that the saccade was expected to bring for the following action. Sensitivity to information gain correlates with the monkeys' efficiency at processing the information in the post-saccadic fixation, but is independent of neuronal reward sensitivity. Reward sensitivity, in turn, is unreliable across task contexts, inconsistent with the view that the cells encode economic utility. The findings suggest that parietal cells involved in oculomotor decisions show uncertainty-dependent boosts of neural gain that facilitate the implementation of active sampling policies, including the selection of relevant cues and the efficient use of the information delivered by these cues.

Intrinsically motivated oculomotor exploration guided by uncertainty reduction and conditioned reinforcement in non-human primates.

Intelligent animals have a high degree of curiosity--the intrinsic desire to know--but the mechanisms of curiosity are poorly understood. A key open question pertains to the internal valuation systems that drive curiosity. What are the cognitive and emotional factors that motivate animals to seek information when this is not reinforced by instrumental rewards? Using a novel oculomotor paradigm, combined with reinforcement learning (RL) simulations, we show that monkeys are intrinsically motivated to search for and look at reward-predictive cues, and that their intrinsic motivation is shaped by a desire to reduce uncertainty, a desire to obtain conditioned reinforcement from positive cues, and individual variations in decision strategy and the cognitive costs of acquiring information. The results suggest that free-viewing oculomotor behavior reveals cognitive and emotional factors underlying the curiosity driven sampling of information.

The subjective visual vertical in a nonhuman primate.

We perceive the visual world as upright as our visual system used information on the orientation of the body to update the internal representation of the visual scene. In humans, this updating is not perfect, thus leading to distortions of the subjective visual vertical. For small roll-tilt angles (<60 degrees ), subjects overestimate the body tilt (E-effect), whereas for larger angles they underestimate it (A-effect). We wanted to know if monkeys show comparable perceptual distortions as they might help to identify the neural basis of a tilt-independent representation of visual objects at the level of single neurons. In order to answer this question, we trained two monkeys to align an arrow with an upright world-centered reference line whose visibility was varied between trials. Trials were performed at roll-tilt angles chosen from -90 degrees to 90 degrees . The monkeys' responses were precise for trials in which the reference line was visible. However, for the trials in which there was no reference line, their responses reflected an overestimation of body tilt (E-effect-like) very similar to humans. Our ability to demonstrate similar visuo-vestibular illusions in monkeys and man is an important step towards understanding the neural mechanism responsible for the perception of an upright visual world.