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.

Task-specific response strategy selection on the basis of recent training experience.

The goal of training is to produce learning for a range of activities that are typically more general than the training task itself. Despite a century of research, predicting the scope of learning from the content of training has proven extremely difficult, with the same task producing narrowly focused learning strategies in some cases and broadly scoped learning strategies in others. Here we test the hypothesis that human subjects will prefer a decision strategy that maximizes performance and reduces uncertainty given the demands of the training task and that the strategy chosen will then predict the extent to which learning is transferable. To test this hypothesis, we trained subjects on a moving dot extrapolation task that makes distinct predictions for two types of learning strategy: a narrow model-free strategy that learns an input-output mapping for training stimuli, and a general model-based strategy that utilizes humans' default predictive model for a class of trajectories. When the number of distinct training trajectories is low, we predict better performance for the mapping strategy, but as the number increases, a predictive model is increasingly favored. Consonant with predictions, subject extrapolations for test trajectories were consistent with using a mapping strategy when trained on a small number of training trajectories and a predictive model when trained on a larger number. The general framework developed here can thus be useful both in interpreting previous patterns of task-specific versus task-general learning, as well as in building future training paradigms with certain desired outcomes.

Differences in perceptual learning transfer as a function of training task.

A growing body of research--including results from behavioral psychology, human structural and functional imaging, single-cell recordings in nonhuman primates, and computational modeling--suggests that perceptual learning effects are best understood as a change in the ability of higher-level integration or association areas to read out sensory information in the service of particular decisions. Work in this vein has argued that, depending on the training experience, the "rules" for this read-out can either be applicable to new contexts (thus engendering learning generalization) or can apply only to the exact training context (thus resulting in learning specificity). Here we contrast learning tasks designed to promote either stimulus-specific or stimulus-general rules. Specifically, we compare learning transfer across visual orientation following training on three different tasks: an orientation categorization task (which permits an orientation-specific learning solution), an orientation estimation task (which requires an orientation-general learning solution), and an orientation categorization task in which the relevant category boundary shifts on every trial (which lies somewhere between the two tasks above). While the simple orientation-categorization training task resulted in orientation-specific learning, the estimation and moving categorization tasks resulted in significant orientation learning generalization. The general framework tested here--that task specificity or generality can be predicted via an examination of the optimal learning solution--may be useful in building future training paradigms with certain desired outcomes.

Auditory frequency and intensity discrimination explained using a cortical population rate code.

The nature of the neural codes for pitch and loudness, two basic auditory attributes, has been a key question in neuroscience for over century. A currently widespread view is that sound intensity (subjectively, loudness) is encoded in spike rates, whereas sound frequency (subjectively, pitch) is encoded in precise spike timing. Here, using information-theoretic analyses, we show that the spike rates of a population of virtual neural units with frequency-tuning and spike-count correlation characteristics similar to those measured in the primary auditory cortex of primates, contain sufficient statistical information to account for the smallest frequency-discrimination thresholds measured in human listeners. The same population, and the same spike-rate code, can also account for the intensity-discrimination thresholds of humans. These results demonstrate the viability of a unified rate-based cortical population code for both sound frequency (pitch) and sound intensity (loudness), and thus suggest a resolution to a long-standing puzzle in auditory neuroscience.

Multisensory decision-making in rats and humans.

We report a novel multisensory decision task designed to encourage subjects to combine information across both time and sensory modalities. We presented subjects, humans and rats, with multisensory event streams, consisting of a series of brief auditory and/or visual events. Subjects made judgments about whether the event rate of these streams was high or low. We have three main findings. First, we report that subjects can combine multisensory information over time to improve judgments about whether a fluctuating rate is high or low. Importantly, the improvement we observed was frequently close to, or better than, the statistically optimal prediction. Second, we found that subjects showed a clear multisensory enhancement both when the inputs in each modality were redundant and when they provided independent evidence about the rate. This latter finding suggests a model where event rates are estimated separately for each modality and fused at a later stage. Finally, because a similar multisensory enhancement was observed in both humans and rats, we conclude that the ability to optimally exploit sequentially presented multisensory information is not restricted to a particular species.

Information-Theoretic Neural Decoding Reproduces Several Laws of Human Behavior.

Human response times conform to several regularities including the Hick-Hyman law, the power law of practice, speed-accuracy trade-offs, and the Stroop effect. Each of these has been thoroughly modeled in isolation, but no account describes these phenomena as predictions of a unified framework. We provide such a framework and show that the phenomena arise as decoding times in a simple neural rate code with an entropy stopping threshold. Whereas traditional information-theoretic encoding systems exploit task statistics to optimize encoding strategies, we move this optimization to the decoder, treating it as a Bayesian ideal observer that can track transmission statistics as prior information during decoding. Our approach allays prominent concerns that applying information-theoretic perspectives to modeling brain and behavior requires complex encoding schemes that are incommensurate with neural encoding.

Decoding Depression Severity From Intracranial Neural Activity.

BACKGROUND: Disorders of mood and cognition are prevalent, disabling, and notoriously difficult to treat. Fueling this challenge in treatment is a significant gap in our understanding of their neurophysiological basis. METHODS: We recorded high-density neural activity from intracranial electrodes implanted in depression-relevant prefrontal cortical regions in 3 human subjects with severe depression. Neural recordings were labeled with depression severity scores across a wide dynamic range using an adaptive assessment that allowed sampling with a temporal frequency greater than that possible with typical rating scales. We modeled these data using regularized regression techniques with region selection to decode depression severity from the prefrontal recordings. RESULTS: Across prefrontal regions, we found that reduced depression severity is associated with decreased low-frequency neural activity and increased high-frequency activity. When constraining our model to decode using a single region, spectral changes in the anterior cingulate cortex best predicted depression severity in all 3 subjects. Relaxing this constraint revealed unique, individual-specific sets of spatiospectral features predictive of symptom severity, reflecting the heterogeneous nature of depression. CONCLUSIONS: The ability to decode depression severity from neural activity increases our fundamental understanding of how depression manifests in the human brain and provides a target neural signature for personalized neuromodulation therapies.

How haptic size sensations improve distance perception.

Determining distances to objects is one of the most ubiquitous perceptual tasks in everyday life. Nevertheless, it is challenging because the information from a single image confounds object size and distance. Though our brains frequently judge distances accurately, the underlying computations employed by the brain are not well understood. Our work illuminates these computions by formulating a family of probabilistic models that encompass a variety of distinct hypotheses about distance and size perception. We compare these models' predictions to a set of human distance judgments in an interception experiment and use Bayesian analysis tools to quantitatively select the best hypothesis on the basis of its explanatory power and robustness over experimental data. The central question is: whether, and how, human distance perception incorporates size cues to improve accuracy. Our conclusions are: 1) humans incorporate haptic object size sensations for distance perception, 2) the incorporation of haptic sensations is suboptimal given their reliability, 3) humans use environmentally accurate size and distance priors, 4) distance judgments are produced by perceptual "posterior sampling". In addition, we compared our model's estimated sensory and motor noise parameters with previously reported measurements in the perceptual literature and found good correspondence between them. Taken together, these results represent a major step forward in establishing the computational underpinnings of human distance perception and the role of size information.

An optimal feedback control framework for grasping objects with position uncertainty.

As we move, the relative location between our hands and objects changes in uncertain ways due to noisy motor commands and imprecise and ambiguous sensory information. The impressive capabilities humans display for interacting and manipulating objects with position uncertainty suggest that our brain maintains representations of location uncertainty and builds compensation for uncertainty into its motor control strategies. Our previous work demonstrated that specific control strategies are used to compensate for location uncertainty. However, it is an open question whether compensation for position uncertainty in grasping is consistent with the stochastic optimal feedback control, mainly due to the difficulty of modeling natural tasks within this framework. In this study, we develop a stochastic optimal feedback control model to evaluate the optimality of human grasping strategies. We investigate the properties of the model through a series of simulation experiments and show that it explains key aspects of previously observed compensation strategies. It also provides a basis for individual differences in terms of differential control costs-the controller compensates only to the extent that performance benefits in terms of making stable grasps outweigh the additional control costs of compensation. These results suggest that stochastic optimal feedback control can be used to understand uncertainty compensation in complex natural tasks like grasping.

Within- and cross-modal distance information disambiguate visual size-change perception.

Perception is fundamentally underconstrained because different combinations of object properties can generate the same sensory information. To disambiguate sensory information into estimates of scene properties, our brains incorporate prior knowledge and additional "auxiliary" (i.e., not directly relevant to desired scene property) sensory information to constrain perceptual interpretations. For example, knowing the distance to an object helps in perceiving its size. The literature contains few demonstrations of the use of prior knowledge and auxiliary information in combined visual and haptic disambiguation and almost no examination of haptic disambiguation of vision beyond "bistable" stimuli. Previous studies have reported humans integrate multiple unambiguous sensations to perceive single, continuous object properties, like size or position. Here we test whether humans use visual and haptic information, individually and jointly, to disambiguate size from distance. We presented participants with a ball moving in depth with a changing diameter. Because no unambiguous distance information is available under monocular viewing, participants rely on prior assumptions about the ball's distance to disambiguate their -size percept. Presenting auxiliary binocular and/or haptic distance information augments participants' prior distance assumptions and improves their size judgment accuracy-though binocular cues were trusted more than haptic. Our results suggest both visual and haptic distance information disambiguate size perception, and we interpret these results in the context of probabilistic perceptual reasoning.

Grasping objects with environmentally induced position uncertainty.

Due to noisy motor commands and imprecise and ambiguous sensory information, there is often substantial uncertainty about the relative location between our body and objects in the environment. Little is known about how well people manage and compensate for this uncertainty in purposive movement tasks like grasping. Grasping objects requires reach trajectories to generate object-fingers contacts that permit stable lifting. For objects with position uncertainty, some trajectories are more efficient than others in terms of the probability of producing stable grasps. We hypothesize that people attempt to generate efficient grasp trajectories that produce stable grasps at first contact without requiring post-contact adjustments. We tested this hypothesis by comparing human uncertainty compensation in grasping objects against optimal predictions. Participants grasped and lifted a cylindrical object with position uncertainty, introduced by moving the cylinder with a robotic arm over a sequence of 5 positions sampled from a strongly oriented 2D Gaussian distribution. Preceding each reach, vision of the object was removed for the remainder of the trial and the cylinder was moved one additional time. In accord with optimal predictions, we found that people compensate by aligning the approach direction with covariance angle to maintain grasp efficiency. This compensation results in higher probability to achieve stable grasps at first contact than non-compensation strategies in grasping objects with directional position uncertainty, and the results provide the first demonstration that humans compensate for uncertainty in a complex purposive task.

A How-to-Model Guide for Neuroscience.

Within neuroscience, models have many roles, including driving hypotheses, making assumptions explicit, synthesizing knowledge, making experimental predictions, and facilitating applications to medicine. While specific modeling techniques are often taught, the process of constructing models for a given phenomenon or question is generally left opaque. Here, informed by guiding many students through modeling exercises at our summer school in CoSMo (Computational Sensory-Motor Neuroscience), we provide a practical 10-step breakdown of the modeling process. This approach makes choices and criteria more explicit and replicable. Experiment design has long been taught in neuroscience; the modeling process should receive the same attention.

Humans trade off viewing time and movement duration to improve visuomotor accuracy in a fast reaching task.

Previous research has shown that the brain uses statistical knowledge of both sensory and motor accuracy to optimize behavioral performance. Here, we present the results of a novel experiment in which participants could control both of these quantities at once. Specifically, maximum performance demanded the simultaneous choices of viewing and movement durations, which directly impacted visual and motor accuracy. Participants reached to a target indicated imprecisely by a two-dimensional distribution of dots within a 1200 ms time limit. By choosing when to reach, participants selected the quality of visual information regarding target location as well as the remaining time available to execute the reach. New dots, and consequently more visual information, appeared until the reach was initiated; after reach initiation, no new dots appeared. However, speed accuracy trade-offs in motor control make early reaches (much remaining time) precise and late reaches (little remaining time) imprecise. Based on each participant's visual- and motor-only target-hitting performances, we computed an "ideal reacher" that selects reach initiation times that minimize predicted reach endpoint deviations from the true target location. The participant's timing choices were qualitatively consistent with ideal predictions: choices varied with stimulus changes (but less than the predicted magnitude) and resulted in near-optimal performance despite the absence of direct feedback defining ideal performance. Our results suggest visual estimates, and their respective accuracies are passed to motor planning systems, which in turn predict the precision of potential reaches and control viewing and movement timing to favorably trade off visual and motor accuracy.

Perceptual multistability predicted by search model for Bayesian decisions.

Perceptual multistability refers to the phenomenon of spontaneous perceptual switching between two or more likely interpretations of an image. Although frequently explained by processes of adaptation or hysteresis, we show that perceptual switching can arise as a natural byproduct of perceptual decision making based on probabilistic (Bayesian) inference, which interprets images by combining probabilistic models of image formation with knowledge of scene regularities. Empirically, we investigated the effect of introducing scene regularities on Necker cube bistability by flanking the Necker cube with fields of unambiguous cubes that are oriented to coincide with one of the Necker cube percepts. We show that background cubes increase the time spent in percepts most similar to the background. To characterize changes in the temporal dynamics of the perceptual alternations beyond percept durations, we introduce Markov Renewal Processes (MRPs). MRPs provide a general mathematical framework for describing probabilistic switching behavior in finite state processes. Additionally, we introduce a simple theoretical model consistent with Bayesian models of vision that involves searching for good interpretations of an image by sampling a posterior distribution coupled with a decay process that favors recent to old interpretations. The model has the same quantitative characteristics as our human data and variation in model parameters can capture between-subject variation. Because the model produces the same kind of stochastic process found in human perceptual behavior, we conclude that multistability may represent an unavoidable by-product of normal perceptual (Bayesian) decision making with ambiguous images.

Variability in stepping direction explains the veering behavior of blind walkers.

Walking without vision results in veering, an inability to maintain a straight path that has important consequences for blind pedestrians. In this study, the authors addressed whether the source of veering in the absence of visual and auditory feedback is better attributed to errors in perceptual encoding or undetected motor error. Three experiments had the following results: No significant differences in the shapes of veering trajectories were found between blind and blindfolded participants; accuracy in detecting curved walking paths was not correlated with simple measures of veering behavior; and explicit perceptual cues to initial walking direction did not reduce veering. The authors present a model that accounts for the major characteristics of participants' veering behavior by postulating 3 independent sources of undetected motor error: initial orientation, consistent biases in step direction, and, most important, variable error in individual steps.

Is prior knowledge of object geometry used in visually guided reaching?

We investigated whether humans use prior knowledge of the geometry of faces in visually guided reaching. When viewing the inside of a mask of a face, the mask is often perceived as being a normal (convex) face, instead of the veridical, hollow (concave) shape. In this "hollow-face illusion," prior knowledge of the shape of faces dominates perception, even when in conflict with information from binocular disparity. Computer images of normal and hollow faces were presented, such that depth information from binocular disparity was consistent or in conflict with prior knowledge of the geometry. Participants reached to touch either the nose or cheek of the faces or gave verbal estimates of the corresponding distances. We found that reaching to touch was dominated by prior knowledge of face geometry. However, hollow faces were estimated to be flatter than normal faces. This suggests that the visual system combines binocular disparity and prior assumptions, rather than completely discounting one or the other. When comparing the magnitude of the hollow-face illusion in reaching and verbal tasks, we found that the flattening effect of the illusion was similar for verbal and reaching tasks.

Revealing individual differences in strategy selection through visual motion extrapolation.

Humans are constantly challenged to make use of internal models to fill in missing sensory information. We measured human performance in a simple motion extrapolation task where no feedback was provided in order to elucidate the models of object motion incorporated into observers' extrapolation strategies. There was no "right" model for extrapolation in this task. Observers consistently adopted one of two models, linear or quadratic, but different observers chose different models. We further demonstrate that differences in motion sensitivity impact the choice of internal models for many observers. These results demonstrate that internal models and individual differences in those models can be elicited by unconstrained, predictive-based psychophysical tasks.

Combining path integration and remembered landmarks when navigating without vision.

This study investigated the interaction between remembered landmark and path integration strategies for estimating current location when walking in an environment without vision. We asked whether observers navigating without vision only rely on path integration information to judge their location, or whether remembered landmarks also influence judgments. Participants estimated their location in a hallway after viewing a target (remembered landmark cue) and then walking blindfolded to the same or a conflicting location (path integration cue). We found that participants averaged remembered landmark and path integration information when they judged that both sources provided congruent information about location, which resulted in more precise estimates compared to estimates made with only path integration. In conclusion, humans integrate remembered landmarks and path integration in a gated fashion, dependent on the congruency of the information. Humans can flexibly combine information about remembered landmarks with path integration cues while navigating without visual information.

Visual motion and the perception of surface material.

Many critical perceptual judgments, from telling whether fruit is ripe to determining whether the ground is slippery, involve estimating the material properties of surfaces. Very little is known about how the brain recognizes materials, even though the problem is likely as important for survival as navigating or recognizing objects. Though previous research has focused nearly exclusively on the properties of static images, recent evidence suggests that motion may affect the appearance of surface material. However, what kind of information motion conveys and how this information may be used by the brain is still unknown. Here, we identify three motion cues that the brain could rely on to distinguish between matte and shiny surfaces. We show that these motion measurements can override static cues, leading to dramatic changes in perceived material depending on the image motion characteristics. A classifier algorithm based on these cues correctly predicts both successes and some striking failures of human material perception. Together these results reveal a previously unknown use for optic flow in the perception of surface material properties.

Effects of visual uncertainty on grasping movements.

To successfully lift an object, a person's fingers must be moved to locations where forces can be applied that are sufficient for maintaining contact and that allow for easy object manipulation. Obtaining such finger positions becomes more difficult when there is perceptual uncertainty about the location of the hand and object. However, knowledge about the amount of uncertainty could be incorporated into grasp plans to mitigate its effect. For example, during peripheral viewing the fingers could open wider to avoid colliding with or missing the object. The goal of this study is to determine the degree to which people incorporate their understanding of visual uncertainty when making a precision grasp. To investigate, subjects reached to a spatially fixed object whose retinal location was varied by fixating points 0-80 degrees to the left of the object. This manipulation controlled the visual uncertainty of the hand and target without affecting the kinematic demands of the task. We found that people systematically changed their grasping behavior as a function of the amount of visual uncertainty in the task. Specifically, subjects' maximum grip aperture increased linearly with target eccentricity. Moreover, the effect of visual uncertainty on finger trajectories could be captured by a single dimension of change along an axis. Together, these findings suggest that the sensorimotor system estimates visual uncertainty and behaviorally adjusts for it during grasping movements.