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

Sports Fans ◽

Perceptual Decision ◽

Amygdala Activity ◽

Sensory Evidence ◽

Human Participants

AbstractPeople 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.

Behavioural and neural signatures of perceptual decision-making are modulated by pupil-linked arousal

eLife ◽

10.7554/elife.42541 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 13

Author(s):

Jochem van Kempen ◽

Gerard M Loughnane ◽

Daniel P Newman ◽

Simon P Kelly ◽

Alexander Thiele ◽

...

Keyword(s):

Decision Making ◽

Sensory Processing ◽

Pupil Diameter ◽

Target Selection ◽

Reaction Times ◽

Perceptual Decision ◽

Attentional Engagement ◽

Processing Steps

The timing and accuracy of perceptual decision-making is exquisitely sensitive to fluctuations in arousal. Although extensive research has highlighted the role of various neural processing stages in forming decisions, our understanding of how arousal impacts these processes remains limited. Here we isolated electrophysiological signatures of decision-making alongside signals reflecting target selection, attentional engagement and motor output and examined their modulation as a function of tonic and phasic arousal, indexed by baseline and task-evoked pupil diameter, respectively. Reaction times were shorter on trials with lower tonic, and higher phasic arousal. Additionally, these two pupil measures were predictive of a unique set of EEG signatures that together represent multiple information processing steps of decision-making. Finally, behavioural variability associated with fluctuations in tonic and phasic arousal, indicative of neuromodulators acting on multiple timescales, was mediated by its effects on the EEG markers of attentional engagement, sensory processing and the variability in decision processing.

Separable neural signatures of confidence during perceptual decisions

10.1101/2021.04.08.439033 ◽

2021 ◽

Author(s):

T. Balsdon ◽

P. Mamassian ◽

V. Wyart

Keyword(s):

Decision Making ◽

Neural Circuit ◽

Spectral Power ◽

Brain Activity ◽

Neural Representation ◽

Perceptual Decision ◽

Electrical Brain Activity ◽

Sensory Evidence ◽

Human Participants

AbstractPerceptual confidence is an evaluation of the validity of perceptual decisions. While there is behavioural evidence that confidence evaluation differs from perceptual decision-making, disentangling these two processes remains a challenge at the neural level. Here we examined the electrical brain activity of human participants in a protracted perceptual decision-making task where observers tend to commit to perceptual decisions early whilst continuing to monitor sensory evidence for evaluating confidence. Premature decision commitments were revealed by patterns of spectral power overlying motor cortex, followed by an attenuation of the neural representation of perceptual decision evidence. A distinct neural representation was associated with suboptimalities affecting confidence reports, with sources localised in the superior parietal and orbitofrontal cortices. In agreement with a dissociation between perception and confidence, these neural resources were recruited even after observers committed to their perceptual decisions, and thus delineate an integral neural circuit for the computation of confidence.

Mesoscale cortical dynamics reflect the interaction of sensory evidence and temporal expectation during perceptual decision-making

Neuron ◽

10.1016/j.neuron.2021.03.031 ◽

2021 ◽

Author(s):

Ivana Orsolic ◽

Maxime Rio ◽

Thomas D. Mrsic-Flogel ◽

Petr Znamenskiy

Keyword(s):

Decision Making ◽

Cortical Dynamics ◽

Perceptual Decision ◽

Temporal Expectation ◽

Flexible categorization in perceptual decision making

Nature Communications ◽

10.1038/s41467-021-21501-z ◽

2021 ◽

Vol 12 (1) ◽

Cited By ~ 1

Author(s):

Genís Prat-Ortega ◽

Klaus Wimmer ◽

Alex Roxin ◽

Jaime de la Rocha

Keyword(s):

Decision Making ◽

Network Models ◽

Drift Diffusion Model ◽

Drift Diffusion ◽

Perceptual Decision ◽

Attractor Dynamics ◽

Attractor Model ◽

Sensory Evidence ◽

Winner Take All

AbstractPerceptual decisions rely on accumulating sensory evidence. This computation has been studied using either drift diffusion models or neurobiological network models exhibiting winner-take-all attractor dynamics. Although both models can account for a large amount of data, it remains unclear whether their dynamics are qualitatively equivalent. Here we show that in the attractor model, but not in the drift diffusion model, an increase in the stimulus fluctuations or the stimulus duration promotes transitions between decision states. The increase in the number of transitions leads to a crossover between weighting mostly early evidence (primacy) to weighting late evidence (recency), a prediction we validate with psychophysical data. Between these two limiting cases, we found a novel flexible categorization regime, in which fluctuations can reverse initially-incorrect categorizations. This reversal asymmetry results in a non-monotonic psychometric curve, a distinctive feature of the attractor model. Our findings point to correcting decision reversals as an important feature of perceptual decision making.

Integration of sensory evidence and reward expectation in mouse perceptual decision-making task with various sensory uncertainties.

iScience ◽

10.1016/j.isci.2021.102826 ◽

2021 ◽

pp. 102826

Author(s):

Akihiro Funamizu

Keyword(s):

Decision Making ◽

Perceptual Decision ◽

Decoupling sensory from decisional choice biases in perceptual decision making

10.1101/062380 ◽

2016 ◽

Author(s):

Daniel Linares ◽

David Aguilar-Lleyda ◽

Joan López-Moliner

Keyword(s):

Decision Making ◽

Theory Model ◽

Decision Makers ◽

Perceptual Decision ◽

Response Mapping ◽

Task Instructions ◽

Detection Theory Model ◽

Sensory Evidence ◽

Choice Bias

ABSTRACTThe contribution of sensory and decisional processes to perceptual decision making is still unclear, even in simple perceptual tasks. When decision makers need to select an action from a set of balanced alternatives, any tendency to choose one alternative more often— choice bias—is consistent with a bias in the sensory evidence, but also with a preference to select that alternative independently of the sensory evidence. To decouple sensory from decisional biases, here we asked humans to perform a simple perceptual discrimination task with two symmetric alternatives under two different task instructions. The instructions varied the response mapping between perception and the category of the alternatives. We found that from 32 participants, 30 exhibited sensory biases and 15 decisional biases. The decisional biases were consistent with a criterion change in a simple signal detection theory model. Perceptual decision making, thus, even in simple scenarios, is affected by sensory and decisional choice biases.IMPACT STATEMENTPerceptual decision making, even in simple scenarios, is affected by sensory and decisional choice biases.

P2-16: Dual-Bound Model and the Role of Time Bound in Perceptual Decision Making

i-Perception ◽

10.1068/if676 ◽

2012 ◽

Vol 3 (9) ◽

pp. 676-676

Author(s):

Daeseob Lim ◽

Hansem Sohn ◽

Sang-Hun Lee

Keyword(s):

Decision Making ◽

Perceptual Decision ◽

Dual Bound

Slow drift of neural activity as a signature of impulsivity in macaque visual and prefrontal cortex

10.1101/2020.01.10.902403 ◽

2020 ◽

Cited By ~ 2

Author(s):

Benjamin R. Cowley ◽

Adam C. Snyder ◽

Katerina Acar ◽

Ryan C. Williamson ◽

Byron M. Yu ◽

...

Keyword(s):

Decision Making ◽

Prefrontal Cortex ◽

Neural Activity ◽

Internal State ◽

Sensory Stimulus ◽

Population Activity ◽

Perceptual Decision ◽

Slow Drift ◽

AbstractAn animal’s decision depends not only on incoming sensory evidence but also on its fluctuating internal state. This internal state is a product of cognitive factors, such as fatigue, motivation, and arousal, but it is unclear how these factors influence the neural processes that encode the sensory stimulus and form a decision. We discovered that, over the timescale of tens of minutes during a perceptual decision-making task, animals slowly shifted their likelihood of reporting stimulus changes. They did this unprompted by task conditions. We recorded neural population activity from visual area V4 as well as prefrontal cortex, and found that the activity of both areas slowly drifted together with the behavioral fluctuations. We reasoned that such slow fluctuations in behavior could either be due to slow changes in how the sensory stimulus is processed or due to a process that acts independently of sensory processing. By analyzing the recorded activity in conjunction with models of perceptual decision-making, we found evidence for the slow drift in neural activity acting as an impulsivity signal, overriding sensory evidence to dictate the final decision. Overall, this work uncovers an internal state embedded in the population activity across multiple brain areas, hidden from typical trial-averaged analyses and revealed only when considering the passage of time within each experimental session. Knowledge of this cognitive factor was critical in elucidating how sensory signals and the internal state together contribute to the decision-making process.

An accumulation-of-evidence task using visual pulses for mice navigating in virtual reality

10.1101/232702 ◽

2017 ◽

Author(s):

Lucas Pinto ◽

Sue Ann Koay ◽

Ben Engelhard ◽

Alice M. Yoon ◽

Ben Deverett ◽

...

Keyword(s):

Decision Making ◽

Virtual Reality ◽

Single Pulse ◽

Model Organisms ◽

Perceptual Decision ◽

Crucial Component ◽

Wide Availability ◽

Multiple Pulses ◽

ABSTRACTThe gradual accumulation of sensory evidence is a crucial component of perceptual decision making, but its neural mechanisms are still poorly understood. Given the wide availability of genetic and optical tools for mice, they can be useful model organisms for the study of these phenomena; however, behavioral tools are largely lacking. Here, we describe a new evidence-accumulation task for head-fixed mice navigating in a virtual reality environment. As they navigate down the stem of a virtual T-maze, they see brief pulses of visual evidence on either side, and retrieve a reward on the arm with the highest number of pulses. The pulses occur randomly with Poisson statistics, yielding a diverse yet well-controlled stimulus set, making the data conducive to a variety of computational approaches. A large number of mice of different genotypes were able to learn and consistently perform the task, at levels similar to rats in analogous tasks. They are sensitive to side differences of a single pulse, and their memory of the cues is stable over time. Moreover, using non-parametric as well as modeling approaches, we show that the mice indeed accumulate evidence: they use multiple pulses of evidence from throughout the cue region of the maze to make their decision, albeit with a small overweighting of earlier cues, and their performance is affected by the magnitude but not the duration of evidence. Additionally, analysis of the mice's running patterns revealed that trajectories are fairly stereotyped yet modulated by the amount of sensory evidence, suggesting that the navigational component of this task may provide a continuous readout correlated to the underlying cognitive variables. Our task, which can be readily integrated with state-of-the-art techniques, is thus a valuable tool to study the circuit mechanisms and dynamics underlying perceptual decision making, particularly under more complex behavioral contexts.