A rodent paradigm for studying perceptual decisions under asymmetric reward

Midbrain Dopamine Neurons Signal Belief in Choice Accuracy during a Perceptual Decision

Recent neuroimaging work has demonstrated that the ventral striatum (VS) encodes confidence in perceptual decisions. However, it remains unclear whether perceptual uncertainty can signal the need to adapt behavior (such as by responding more cautiously) and whether such behavioral changes are related to uncertainty-dependent activity within the VS. Changes in response strategy have previously been observed following errors and are associated with both medial frontal cortex (MFC) and VS, two components of the performance-monitoring network. If uncertainty can elicit changes in response strategy (slowing), then one might hypothesize that these changes rely on the performance-monitoring network. In the present study, we investigated the link between perceptual uncertainty and task-related behavioral adaptations (response slowing and accuracy increases), as well as how such behavioral changes relate to uncertainty-dependent activity within MFC and VS. Our participants performed a two-choice perceptual decision-making task in which perceptual uncertainty was reported on each trial while behavioral and event-related functional magnetic resonance imaging data were collected. Analysis of the behavioral data revealed that uncertain (but correct) responses led to slowing on subsequent trials, a phenomenon that was positively correlated with increased accuracy. Critically, post-uncertainty slowing was negatively correlated with the VS activity elicited by uncertain responses. In agreement with previous reports, increases in MFC activation were observed for uncertain responses, although MFC activity was not correlated with post-uncertainty slowing. These results suggest that perceptual uncertainty can serve as a signal to adapt one's response strategy and that such behavioral changes are closely tied to the VS, a key node in the performance-monitoring network.

Confidence in a perceptual decision is a subjective estimate of the accuracy of one’s choice. As such, confidence is thought to be an important computation for a variety of cognitive and perceptual processes, and it features heavily in theorizing about conscious access to perceptual states. Recent experiments have revealed a “positive evidence bias” (PEB) in the computations underlying confidence reports. A PEB occurs when confidence, unlike objective choice, overweights the evidence for the correct (or chosen) option, relative to evidence against the correct (or chosen) option. Accordingly, in a perceptual task, appropriate stimulus conditions can be arranged that produce selective changes in confidence reports but no changes in accuracy. Although the PEB is generally assumed to reflect the observer’s perceptual and/or decision processes, post-decisional accounts have not been ruled out. We therefore asked whether the PEB persisted under novel conditions that addressed two possible post-decisional accounts: (i) post-decision evidence accumulation that contributes to a confidence report solicited after the perceptual choice and (ii) a memory bias that emerges in the delay between the stimulus offset and the confidence report. We found that even when the stimulus remained on the screen until observers responded, and when observers reported their choice and confidence simultaneously, the PEB still emerged. Signal detection-based modeling showed that the PEB was not associated with changes to metacognitive efficiency, but rather to confidence criteria. The data show that memory biases cannot explain the PEB and provide evidence against a post-decision evidence accumulation account, bolstering the idea that the PEB is perceptual or decisional in nature.

Atomoxetine and reward size equally improve task engagement and perceptual decisions but differently affect movement execution

Perceptual decisions are typically accompanied by a subjective sense of (un)certainty. There is robust evidence that observers have access to a reliable estimate of their own uncertainty and can judge the validity of their perceptual decisions. However, there is still a debate to what extent these meta-perceptual judgements underly a common mechanism that can monitor perceptual decisions across different sensory modalities. It has been suggested that perceptual confidence can be evaluated on an abstract scale that is not only task-independent but also modality-independent. We aimed to scrutinize these findings by measuring visual contrast and tactile vibration discrimination thresholds in a confidence forced-choice task. A total of 56 participants took part in our study. We determined thresholds for trials in which perceptual decisions were chosen as confident and for those that were declined as confident. Confidence comparisons were made between perceptual decisions either within the visual and tactile modality, respectively, or across both modalities. Furthermore, we assessed executive functions to explore a possible link between cognitive control and meta-perceptual capacities. We found that perceptual performance was a good predictor of confidence judgments and that the threshold modulation was similarly pronounced in both modalities. Most importantly, participants compared their perceptual confidence across visual and tactile decisions with the same precision as within the same modality. Cognitive control capacities were not related to meta-perceptual performance. In conclusion, our findings corroborate that perceptual uncertainty can be accessed on an abstract scale, allowing for confidence comparisons across sensory modalities.

Face-to-face communication relies on the integration of acoustic speech signals with the corresponding facial articulations. In the McGurk illusion, an auditory /ba/ phoneme presented simultaneously with a facial articulation of a /ga/ (i.e., viseme), is typically fused into an illusory 'da' percept. Despite its widespread use as an index of audiovisual speech integration, critics argue that it arises from perceptual processes that differ categorically from natural speech recognition. Conversely, Bayesian theoretical frameworks suggest that both the illusory McGurk and the veridical audiovisual congruent speech percepts result from probabilistic inference based on noisy sensory signals. According to these models, the inter-sensory conflict in McGurk stimuli may only increase observers' perceptual uncertainty. This functional magnetic resonance imaging (fMRI) study presented participants (20 male and 24 female) with audiovisual congruent, McGurk (i.e., auditory /ba/ + visual /ga/), and incongruent (i.e., auditory /ga/ + visual /ba/) stimuli along with their unisensory counterparts in a syllable categorization task. Behaviorally, observers' response entropy was greater for McGurk compared to congruent audiovisual stimuli. At the neural level, McGurk stimuli increased activations in a widespread neural system, extending from the inferior frontal sulci (IFS) to the pre-supplementary motor area (pre-SMA) and insulae, typically involved in cognitive control processes. Crucially, in line with Bayesian theories these activation increases were fully accounted for by observers' perceptual uncertainty as measured by their response entropy. Our findings suggest that McGurk and congruent speech processing rely on shared neural mechanisms, thereby supporting the McGurk illusion as a valid measure of natural audiovisual speech perception.

Although the decisions of our daily lives often occur in the context of temporal and reward structures, the impact of such regularities on decision-making strategy is poorly understood. Here, to explore how temporal and reward context modulate strategy, we trained 2 male rhesus monkeys to perform a novel perceptual decision-making task with asymmetric rewards and time-varying evidence reliability. To model the choice and response time patterns, we developed a computational framework for fitting generalized drift-diffusion models, which flexibly accommodate diverse evidence accumulation strategies. We found that a dynamic urgency signal and leaky integration, in combination with two independent forms of reward biases, best capture behavior. We also tested how temporal structure influences urgency by systematically manipulating the temporal structure of sensory evidence, and found that the time course of urgency was affected by temporal context. Overall, our approach identified key components of cognitive mechanisms for incorporating temporal and reward structure into decisions.SIGNIFICANCE STATEMENT In everyday life, decisions are influenced by many factors, including reward structures and stimulus timing. While reward and timing have been characterized in isolation, ecologically valid decision-making involves a multiplicity of factors acting simultaneously. This raises questions about whether the same decision-making strategy is used when these two factors are concurrently manipulated. To address these questions, we trained rhesus monkeys to perform a novel decision-making task with both reward asymmetry and temporal uncertainty. In order to understand their strategy and hint at its neural mechanisms, we used the new generalized drift diffusion modeling framework to model both reward and timing mechanisms. We found two of each reward and timing mechanisms are necessary to explain our data.

Sensory and environmental uncertainty in perceptual decision-making

Decision Making in Recurrent Neuronal Circuits

Discretion for behavioral selection affects development of habit formation after extended training in rats

Well over half a century ago, Benjamin Lee Whorf [Carroll JB (1956) Language, Thought, and Reality: Selected Writings of Benjamin Lee Whorf (MIT Press, Cambridge, MA)] proposed that language affects perception and thought and is used to segment nature, a hypothesis that has since been tested by linguistic and behavioral studies. Although clear Whorfian effects have been found, it has not yet been demonstrated that language influences brain activity associated with perception and/or immediate postperceptual processes (referred hereafter as "perceptual decision"). Here, by using functional magnetic resonance imaging, we show that brain regions mediating language processes participate in neural networks activated by perceptual decision. When subjects performed a perceptual discrimination task on easy-to-name and hard-to-name colored squares, largely overlapping cortical regions were identified, which included areas of the occipital cortex critical for color vision and regions in the bilateral frontal gyrus. Crucially, however, in comparison with hard-to-name colored squares, perceptual discrimination of easy-to-name colors evoked stronger activation in the left posterior superior temporal gyrus and inferior parietal lobule, two regions responsible for word-finding processes, as demonstrated by a localizer experiment that uses an explicit color patch naming task. This finding suggests that the language-processing areas of the brain are directly involved in visual perceptual decision, thus providing neuroimaging support for the Whorf hypothesis.

Response inhibition is a primary executive control function that allows the withholding of inappropriate responses, and requires appropriate perception of the external environment to achieve a behavioral goal. It remains unclear, however, how response inhibition is achieved when goal-relevant information involves perceptual uncertainty. Twenty-six human participants of both sexes performed a go/no-go task where visually presented random-dot motion stimuli involved perceptual uncertainties. The right inferior frontal cortex (rIFC) was involved in response inhibition, and the middle temporal (MT) region showed greater activity when dot motions involved less uncertainty. A neocortical temporal region in the superior temporal sulcus (STS) specifically showed greater activity during response inhibition in more perceptually certain trials. In this STS region, activity was greater when response inhibition was successful than when it failed. Directional effective connectivity analysis revealed that, in more coherent trials, the MT and STS regions showed enhanced connectivity to the rIFC, whereas in less coherent trials, the signal direction was reversed. These results suggest that a reversible fronto-temporal functional network guides response inhibition and perceptual decision-making under perceptual uncertainty, and in this network, perceptual information in the MT is converted to control information in the rIFC via STS, enabling achievement of response inhibition.SIGNIFICANCE STATEMENT Response inhibition refers to withholding inappropriate behavior and is important for achieving goals. Often, however, decision must be made based on limited environmental evidence. We showed that successful response inhibition is guided by a neocortical temporal region that plays a hub role in converting perceived information coded in a posterior temporal region to control information coded in the PFC. Interestingly, when a perceived stimulus becomes more uncertain, the PFC supplements stimulus encoding in the temporal regions. Our results highlight fronto-temporal mechanisms of response inhibition in which conversion of stimulus-control information is regulated based on the uncertainty of environmental evidence.

Flexible adaptation to changing environments is a representative executive control function implicated in the frontoparietal network that requires appropriate extraction of goal-relevant information through perception of the external environment. It remains unclear, however, how the flexibility is achieved under situations where goal-relevant information is uncertain. To address this issue, the current study examined neural mechanisms for task switching in which task-relevant information involved perceptual uncertainty. Twenty-eight human participants of both sexes alternated behavioral tasks in which they judged motion direction or color of visually presented colored dot stimuli that moved randomly. Task switching was associated with frontoparietal regions in the left hemisphere, and perception of ambiguous stimuli involved contralateral homologous frontoparietal regions. On the other hand, in stimulus-modality-dependent occipitotemporal regions, task coding information was increased during task switching. Effective connectivity analysis revealed that the frontal regions signaled toward the modality-dependent occipitotemporal regions when a relevant stimulus was more ambiguous, whereas the occipitotemporal regions signaled toward the frontal regions when the stimulus was more distinctive. These results suggest that complementary prefrontal mechanisms in the left and right hemispheres help to achieve a behavioral goal when the external environment involves perceptual uncertainty.SIGNIFICANCE STATEMENT In our daily life, environmental information to achieve a goal is not always certain, but we make judgments in such situations, and change our behavior accordingly. This study examined how the flexibility of behavior is achieved in a situation where goal-relevant information involves perceptual uncertainty. fMRI revealed that the lateral prefrontal cortex (PFC) in the left hemisphere is associated with behavioral flexibility, and the perception of ambiguous stimuli involves the PFC in the right hemisphere. These bilateral PFC signaled to stimulus-modality-dependent occipitotemporal regions, depending on perceptual uncertainty and the task to be performed. These top-down signals supplement task coding in the occipitotemporal regions, and highlight interhemispheric prefrontal mechanisms involved in executive control and perceptual decision-making.

Bias occurs in perceptual decisions when the reward associated with a particular response dominates the sensory evidence in support of a choice. However, it remains unclear how this bias is acquired and once acquired, how it influences perceptual decision processes in the brain. We addressed these questions using model-based neuroimaging in a motion discrimination paradigm where contextual cues suggested which one of two options would receive higher rewards on each trial. We found that participants gradually learned to choose the higher-rewarded option in each context when making a perceptual decision. The amount of bias on each trial was fit well by a reinforcement-learning model that estimated the subjective value of each option within the current context. The brain mechanisms underlying this bias acquisition process were similar to those observed in reward-based decision tasks: prediction errors correlated with the fMRI signals in ventral striatum, dlPFC, and parietal cortex, whereas the amount of acquired bias correlated with activity in ventromedial prefrontal (vmPFC), dorsolateral frontal (dlPFC), and parietal cortices. Moreover, psychophysiological interaction analysis revealed that as bias increased, functional connectivity increased within multiple brain networks (dlPFC-vmPFC-visual, vmPFC-motor, and parietal-anterior-cingulate), suggesting that multiple mechanisms contribute to bias in perceptual decisions through integration of value processing with action, sensory, and control systems. These provide a novel link between the neural mechanisms underlying perceptual and economic decision-making.

Predictive coding theories state an aberrant weighting of prior beliefs and present sensory information as a core computational pathology in psychosis. Specifically, it has been proposed that the influence of prior beliefs which attenuate improbable sensory information is weakened, resulting in an overweighing of this potentially misleading information. However, it is currently unclear whether this alteration is specific to perceptual processes or whether it represents a more pervasive deficit that extends to cognitive processes. Here, we carried out 2 behavioral experiments that probed the usage of priors during perceptual and cognitive processes, respectively, in 123 healthy individuals with varying degrees of delusion proneness. In an audio-visual perceptual discrimination task, participants had to judge the global motion direction of random dot kinematograms. Prior beliefs were induced by auditory cues that probabilistically predicted the global motion direction of the dot kinematograms, allowing us to measure the impact of prior beliefs on perceptual decision making. A control experiment paralleled the design of the perceptual decision making task in the domain of cognitive decision making. By fitting the participants' responses with a probabilistic decision model, we quantified the impact of prior beliefs on participants' decisions in both tasks. With growing delusion proneness, we found a decreased impact of prior beliefs on perceptual but not on cognitive decision making. Our results show that delusion proneness is linked to a specifically reduced usage of prior beliefs in perceptual decisions, thereby empirically substantiating predictive coding theories of psychosis.