Trial-by-trial fluctuations in amygdala activity track motivational enhancement of desirable sensory evidence during perceptual decision-making

People are biased towards seeing outcomes that they are motivated to see. For example, sports fans of opposing teams often perceive the same ambiguous foul in favor of the team they support. Here, we test the hypothesis that amygdala-dependent allocation of visual attention facilitates motivational biases in perceptual decision-making. Human participants were rewarded for correctly categorizing an ambiguous image into one of two categories while undergoing fMRI. On each trial, we used a financial bonus to motivate participants to see one category over another. The reward maximizing strategy was to perform the categorization task accurately, but participants were biased towards categorizing the images as the category we motivated them to see. Heightened amygdala activity preceded motivation consistent categorizations, and participants with higher amygdala activation exhibited stronger motivational biases in their perceptual reports. Trial-by-trial amygdala activity was associated with stronger enhancement of neural activity encoding desirable percepts in sensory cortices, suggesting that amygdala-dependent effects on perceptual decisions arose from biased sensory processing. Analyses using a drift diffusion model provide converging evidence that trial-by-trial amygdala activity was associated with stronger motivational biases in the accumulation of sensory evidence. Prior work examining biases in perceptual decision-making have focused on the role of frontoparietal regions. Our work highlights an important contribution of the amygdala. When people are motivated to see one outcome over another, the amygdala biases perceptual decisions towards those outcomes.Significance StatementForming accurate perceptions of the environment is essential for adaptive behavior. People however are biased towards seeing what they want to see, giving rise to inaccurate perceptions and erroneous decisions. Here, we combined behavior, modeling, and fMRI to show that the bias towards seeing desirable percepts is related to trial-by-trial fluctuations in amygdala activity. In particular, during moments with higher amygdala activity, sensory processing is biased in favor of desirable percepts, such that participants are more likely to see what they want to see. These findings highlight the role of the amygdala in biasing visual perception, and shed light on the neural mechanisms underlying the influence of motivation and reward on how people decide what they see.

Response-locked classification image analysis of perceptual decision making in contrast detection

In many situations, humans make decisions based on serially sampled information through the observation of visual stimuli. To quantify the critical information used by the observer in such dynamic decision making, we here applied a classification image (CI) analysis locked to the observer's reaction time (RT) in a simple detection task for a luminance target that gradually appeared in dynamic noise. We found that the response-locked CI shows a spatiotemporally biphasic weighting profile that peaked about 300 ms before the response, but this profile substantially varied depending on RT; positive weights dominated at short RTs and negative weights at long RTs. We show that these diverse results are explained by a simple perceptual decision mechanism that accumulates the output of the perceptual process as modelled by a spatiotemporal contrast detector. We discuss possible applications and the limitations of the response-locked CI analysis.

A confirmation bias in perceptual decision-making due to hierarchical approximate inference

Making good decisions requires updating beliefs according to new evidence. This is a dynamical process that is prone to biases: in some cases, beliefs become entrenched and resistant to new evidence (leading to primacy effects), while in other cases, beliefs fade over time and rely primarily on later evidence (leading to recency effects). How and why either type of bias dominates in a given context is an important open question. Here, we study this question in classic perceptual decision-making tasks, where, puzzlingly, previous empirical studies differ in the kinds of biases they observe, ranging from primacy to recency, despite seemingly equivalent tasks. We present a new model, based on hierarchical approximate inference and derived from normative principles, that not only explains both primacy and recency effects in existing studies, but also predicts how the type of bias should depend on the statistics of stimuli in a given task. We verify this prediction in a novel visual discrimination task with human observers, finding that each observer’s temporal bias changed as the result of changing the key stimulus statistics identified by our model. The key dynamic that leads to a primacy bias in our model is an overweighting of new sensory information that agrees with the observer’s existing belief—a type of ‘confirmation bias’. By fitting an extended drift-diffusion model to our data we rule out an alternative explanation for primacy effects due to bounded integration. Taken together, our results resolve a major discrepancy among existing perceptual decision-making studies, and suggest that a key source of bias in human decision-making is approximate hierarchical inference.

Dissociating the Impact of Movement Time and Energy Costs on Decision-Making and Action Initiation in Humans

Recent theories and data suggest that adapted behavior involves economic computations during which multiple trade-offs between reward value, accuracy requirement, energy expenditure, and elapsing time are solved so as to obtain rewards as soon as possible while spending the least possible amount of energy. However, the relative impact of movement energy and duration costs on perceptual decision-making and movement initiation is poorly understood. Here, we tested 31 healthy subjects on a perceptual decision-making task in which they executed reaching movements to report probabilistic choices. In distinct blocks of trials, the reaching duration (“Time” condition) and energy (“Effort” condition) costs were independently varied compared to a “Reference” block, while decision difficulty was maintained similar at the block level. Participants also performed a simple delayed-reaching (DR) task aimed at estimating movement initiation duration in each motor condition. Results in that DR task show that long duration movements extended reaction times (RTs) in most subjects, whereas energy-consuming movements led to mixed effects on RTs. In the decision task, about half of the subjects decreased their decision durations (DDs) in the Time condition, while the impact of energy on DDs were again mixed across subjects. Decision accuracy was overall similar across motor conditions. These results indicate that movement duration and, to a lesser extent, energy expenditure, idiosyncratically affect perceptual decision-making and action initiation. We propose that subjects who shortened their choices in the time-consuming condition of the decision task did so to limit a drop of reward rate.

The Pseudoscientific Structure of “Perceptual Decision-Making” and other “Signal Detection Theory"-based Research (or How Science Works When It Works)

The assumptions and formulas of “Signal Detection Theory” (SDT) dominate psychophysics and neuroscience, and serve as the basis of visual neuroscience under the rubric of “perceptual decision-making.” Here, I discuss how the overly simple, ad hoc assumptions of SDT served to rationalize the chronic failure of traditional psychophysics to achieve reliable results; how the constraints on outcomes imposed by the traditional methods combined with SDT to artificially immunize core assumptions from empirical challenge; and how consequently, research activity has been reduced to a seemingly uncomplicated - yet still non-replicable - matter of mere measurement and correlation. I contrast the structure of this ever-barren approach to the structure of research that respects reality and expands our knowledge of the natural world.

Age-related deficits in rapid visuomotor decision-making

Many goal-directed actions that require rapid visuomotor planning and perceptual decision-making are affected in older adults, causing difficulties in execution of many functional activities of daily living. Visuomotor planning and perceptual decision-making are mediated by the dorsal and ventral visual streams, respectively, but it is unclear how age-induced changes in sensory processing in these streams contribute to declines in goal-directed actions. Previously, we have shown that in healthy adults, task demands influence movement strategies during visuomotor decision-making, reflecting differential integration of sensory information between the two streams. Here, we asked the question if older adults would exhibit larger declines in interactions between the two streams during demanding motor tasks. Older adults (n=15) and young controls (n=26) performed reaching or interception movements towards virtual objects. In some blocks of trials, participants also had to select an appropriate movement goal based on the shape of the object. Our results showed that older adults corrected fewer initial decision errors during both reaching and interception movements. During the interception decision task, older adults made more decision- and execution-related errors than young adults, which were related to early initiation of their movements. Together, these results suggest that older adults have a reduced ability to integrate new perceptual information to guide online action, which may reflect impaired ventral-dorsal stream interactions.