Dendritic Integration of Sensory Evidence in Perceptual Decision-Making.

Perceptual decisions require the accumulation of sensory information to a response criterion. Most accounts of how the brain performs this process of temporal integration have focused on evolving patterns of spiking activity. We report that subthreshold changes in membrane voltage can represent accumulating evidence before a choice. αß core Kenyon cells (αßc KCs) in the mushroom bodies of fruit flies integrate odor-evoked synaptic inputs to action potential threshold at timescales matching the speed of olfactory discrimination. The forkhead box P transcription factor (FoxP) sets neuronal integration and behavioral decision times by controlling the abundance of the voltage-gated potassium channel Shal (KV4) in αßc KC dendrites. αßc KCs thus tailor, through a particular constellation of biophysical properties, the generic process of synaptic integration to the demands of sequential sampling.

Cardiac-Sympathetic Contractility and Neural Alpha-Band Power: Cross-Modal Collaboration during Approach-Avoidance Conflict.

As evidence mounts that the cardiac-sympathetic nervous system reacts to challenging cognitive settings, we ask if these responses are epiphenomenal companions or if there is evidence suggesting a more intertwined role of this system with cognitive function. Healthy male and female human participants performed an approach-avoidance paradigm, trading off monetary reward for painful electric shock, while we recorded simultaneous electroencephalographic and cardiac-sympathetic signals. Participants were reward sensitive but also experienced approach-avoidance "conflict" when the subjective appeal of the reward was near equivalent to the revulsion of the cost. Drift-diffusion model parameters suggested that participants managed conflict in part by integrating larger volumes of evidence into choices (wider decision boundaries). Late alpha-band (neural) dynamics were consistent with widening decision boundaries serving to combat reward sensitivity and spread attention more fairly to all dimensions of available information. Independently, wider boundaries were also associated with cardiac "contractility" (an index of sympathetically mediated positive inotropy). We also saw evidence of conflict-specific "collaboration" between the neural and cardiac-sympathetic signals. In states of high conflict, the alignment (i.e., product) of alpha dynamics and contractility were associated with a further widening of the boundary, independent of either signal's singular association. Cross-trial coherence analyses provided additional evidence that the autonomic systems controlling cardiac-sympathetics might influence the assessment of information streams during conflict by disrupting or overriding reward processing. We conclude that cardiac-sympathetic control might play a critical role, in collaboration with cognitive processes, during the approach-avoidance conflict in humans.

Cortical ß Power Reflects a Neural Implementation of Decision Boundary Collapse in Speeded Decisions.

A prominent account of decision-making assumes that information is accumulated until a fixed response threshold is crossed. However, many decisions require weighting of information appropriately against time. Collapsing response thresholds are a mathematically optimal solution to this decision problem. However, our understanding of the neurocomputational mechanisms underlying dynamic response thresholds remains significantly incomplete. To investigate this issue, we used a multistage drift-diffusion model (DDM) and also analyzed EEG ß power lateralization (BPL). The latter served as a neural proxy for decision signals. We analyzed a large dataset (n = 863; 434 females and 429 males) from a speeded flanker task and data from an independent confirmation sample (n = 119; 70 females and 49 males). We showed that a DDM with collapsing decision thresholds, a process wherein the decision boundary reduces over time, captured participants' time-dependent decision policy more accurately than a model with fixed thresholds. Previous research suggests that BPL over motor cortices reflects features of a decision signal and that its peak, coinciding with the motor response, may serve as a neural proxy for the decision threshold. We show that BPL around the response decreased with increasing RTs. Together, our findings offer compelling evidence for the existence of collapsing decision thresholds in decision-making processes.

Optogenetic Inhibition of Rat Anterior Cingulate Cortex Impairs the Ability to Initiate and Stay on Task.

Our prior research has identified neural correlates of cognitive control in the anterior cingulate cortex (ACC), leading us to hypothesize that the ACC is necessary for increasing attention as rats flexibly learn new contingencies during a complex reward-guided decision-making task. Here, we tested this hypothesis by using optogenetics to transiently inhibit the ACC, while rats of either sex performed the same two-choice task. ACC inhibition had a profound impact on behavior that extended beyond deficits in attention during learning when expected outcomes were uncertain. We found that ACC inactivation slowed and reduced the number of trials rats initiated and impaired both their accuracy and their ability to complete sessions. Furthermore, drift-diffusion model analysis suggested that free-choice performance and evidence accumulation (i.e., reduced drift rates) were degraded during initial learning-leading to weaker associations that were more easily overridden in later trial blocks (i.e., stronger bias). Together, these results suggest that in addition to attention-related functions, the ACC contributes to the ability to initiate trials and generally stay on task.

Empathy incites a stable prosocial decision bias.

Empathy toward suffering individuals serves as potent driver for prosocial behavior. However, it remains unclear whether prosociality induced by empathy for another person's pain persists once that person's suffering diminishes. To test this, participants underwent functional magnetic resonance imaging while performing a binary social decision task that involved allocation of points to themselves and another person. In block one, participants completed the task after witnessing frequent painful stimulation of the other person, and in block two, after observing low frequency of painful stimulation. Drift-diffusion modeling revealed an increased initial bias toward making prosocial decisions in the first block compared with baseline that persisted in the second block. These results were replicated in an independent behavioral study. An additional control study showed that this effect may be specific to empathy as stability was not evident when prosocial decisions were driven by a social norm such as reciprocity. Increased neural activation in dorsomedial prefrontal cortex was linked to empathic concern after witnessing frequent pain and to a general prosocial decision bias after witnessing rare pain. Altogether, our findings show that empathy for pain elicits a stable inclination toward making prosocial decisions even as their suffering diminishes.

Anterior cingulate cortex lesions impair multiple facets of task engagement not mediated by dorsomedial striatum neuron firing.

The anterior cingulate cortex (ACC) has been implicated across multiple highly specialized cognitive functions-including task engagement, motivation, error detection, attention allocation, value processing, and action selection. Here, we ask if ACC lesions disrupt task performance and firing in dorsomedial striatum (DMS) during the performance of a reward-guided decision-making task that engages many of these cognitive functions. We found that ACC lesions impacted several facets of task performance-including decreasing the initiation and completion of trials, slowing reaction times, and resulting in suboptimal and inaccurate action selection. Reductions in movement times towards the end of behavioral sessions further suggested attenuations in motivation, which paralleled reductions in directional action selection signals in the DMS that were observed later in recording sessions. Surprisingly, however, beyond altered action signals late in sessions-neural correlates in the DMS were largely unaffected, even though behavior was disrupted at multiple levels. We conclude that ACC lesions result in overall deficits in task engagement that impact multiple facets of task performance during our reward-guided decision-making task, which-beyond impacting motivated action signals-arise from dysregulated attentional signals in the ACC and are mediated via downstream targets other than DMS.

High-value decisions are fast and accurate, inconsistent with diminishing value sensitivity.

It is a widely held belief that people's choices are less sensitive to changes in value as value increases. For example, the subjective difference between $11 and $12 is believed to be smaller than between $1 and $2. This idea is consistent with applications of the Weber-Fechner Law and divisive normalization to value-based choice and with psychological interpretations of diminishing marginal utility. According to random utility theory in economics, smaller subjective differences predict less accurate choices. Meanwhile, in the context of sequential sampling models in psychology, smaller subjective differences also predict longer response times. Based on these models, we would predict decisions between high-value options to be slower and less accurate. In contrast, some have argued on normative grounds that choices between high-value options should be made with less caution, leading to faster and less accurate choices. Here, we model the dynamics of the choice process across three different choice domains, accounting for both discriminability and response caution. Contrary to predictions, we mostly observe faster and more accurate decisions (i.e., higher drift rates) between high-value options. We also observe that when participants are alerted about incoming high-value decisions, they exert more caution and not less. We rule out several explanations for these results, using tasks with both subjective and objective values. These results cast doubt on the notion that increasing value reduces discriminability.

An Accumulating Neural Signal Underlying Binocular Rivalry Dynamics.

During binocular rivalry, conflicting images are presented one to each eye and perception alternates stochastically between them. Despite stable percepts between alternations, modeling suggests that neural signals representing the two images change gradually, and that the duration of stable percepts are determined by the time required for these signals to reach a threshold that triggers an alternation. However, direct physiological evidence for such signals has been lacking. Here, we identify a neural signal in the human visual cortex that shows these predicted properties. We measured steady-state visual evoked potentials (SSVEPs) in 84 human participants (62 females, 22 males) who were presented with orthogonal gratings, one to each eye, flickering at different frequencies. Participants indicated their percept while EEG data were collected. The time courses of the SSVEP amplitudes at the two frequencies were then compared across different percept durations, within participants. For all durations, the amplitude of signals corresponding to the suppressed stimulus increased and the amplitude corresponding to the dominant stimulus decreased throughout the percept. Critically, longer percepts were characterized by more gradual increases in the suppressed signal and more gradual decreases of the dominant signal. Changes in signals were similar and rapid at the end of all percepts, presumably reflecting perceptual transitions. These features of the SSVEP time courses are well predicted by a model in which perceptual transitions are produced by the accumulation of noisy signals. Identification of this signal underlying binocular rivalry should allow strong tests of neural models of rivalry, bistable perception, and neural suppression.SIGNIFICANCE STATEMENT During binocular rivalry, two conflicting images are presented to the two eyes and perception alternates between them, with switches occurring at seemingly random times. Rivalry is an important and longstanding model system in neuroscience, used for understanding neural suppression, intrinsic neural dynamics, and even the neural correlates of consciousness. All models of rivalry propose that it depends on gradually changing neural activity that on reaching some threshold triggers the perceptual switches. This manuscript reports the first physiological measurement of neural signals with that set of properties in human participants. The signals, measured with EEG in human observers, closely match the predictions of recent models of rivalry, and should pave the way for much future work.

Two fundamentally different mechanisms by which unconscious information impairs behavioral performance: Evidence from fMRI and computational modeling.

It is increasingly clear that unconscious information impairs the performance of the corresponding action when the instruction to act is delayed. However, whether this impairment occurs at the response level or at the perceptual level remains controversial. This study used fMRI and a computational model with a pre-post design to address this elusive issue. The fMRI results showed that when the unconscious information containing strong stimulus-response associations was irrelevant to subsequent stimuli, the precuneus in the parietal lobe, which is thought to be involved in sensorimotor processing, was activated. In contrast, when the unconscious information was relevant to subsequent stimuli, regardless of the strength of the stimulus-response associations, some regions in the occipital and temporal cortices, which are thought to be involved in visual perceptual processing, were activated. In addition, the percent signal change in the regions of interest associated with motor inhibition was modulated by compatibility in the irrelevant but not in the relevant stimuli conditions. Modeling of behavioral data further supported that the irrelevant and relevant stimuli conditions involved fundamentally different mechanisms. Our finding reconciles the debate about the mechanism by which unconscious information impairs action performance and has important implications for understanding of unconscious cognition.

Deep latent variable joint cognitive modeling of neural signals and human behavior.

As the field of computational cognitive neuroscience continues to expand and generate new theories, there is a growing need for more advanced methods to test the hypothesis of brain-behavior relationships. Recent progress in Bayesian cognitive modeling has enabled the combination of neural and behavioral models into a single unifying framework. However, these approaches require manual feature extraction, and lack the capability to discover previously unknown neural features in more complex data. Consequently, this would hinder the expressiveness of the models. To address these challenges, we propose a Neurocognitive Variational Autoencoder (NCVA) to conjoin high-dimensional EEG with a cognitive model in both generative and predictive modeling analyses. Importantly, our NCVA enables both the prediction of EEG signals given behavioral data and the estimation of cognitive model parameters from EEG signals. This novel approach can allow for a more comprehensive understanding of the triplet relationship between behavior, brain activity, and cognitive processes.

Pre-supplementary motor area strengthens reward sensitivity in intertemporal choice.

Previous investigations on the causal neural mechanisms underlying intertemporal decision making focused on the dorsolateral prefrontal cortex as neural substrate of cognitive control. However, little is known, about the causal contributions of further parts of the frontoparietal control network to delaying gratification, including the pre-supplementary motor area (pre-SMA) and posterior parietal cortex (PPC). Conflicting previous evidence related pre-SMA and PPC either to evidence accumulation processes, choice biases, or response caution. To disentangle between these alternatives, we combined drift diffusion models of decision making with online transcranial magnetic stimulation (TMS) over pre-SMA and PPC during an intertemporal decision task. While we observed no robust effects of PPC TMS, perturbation of pre-SMA activity reduced preferences for larger over smaller rewards. A drift diffusion model of decision making suggests that pre-SMA increases the weight assigned to reward magnitudes during the evidence accumulation process without affecting choice biases or response caution. Taken together, the current findings reveal the computational role of the pre-SMA in value-based decision making, showing that pre-SMA promotes choices of larger, costly rewards by strengthening the sensitivity to reward magnitudes.

Rat movements reflect internal decision dynamics in an evidence accumulation task.

Perceptual decision-making involves multiple cognitive processes, including accumulation of sensory evidence, planning, and executing a motor action. How these processes are intertwined is unclear; some models assume that decision-related processes precede motor execution, whereas others propose that movements reflecting on-going decision processes occur before commitment to a choice. Here we combine and apply two complementary methods to study the relationship between decision processes and the movements leading up to a choice. The first is a free response pulse-based evidence accumulation task, in which stimuli continue until choice is reported and the second is a motion-based drift diffusion model (mDDM), in which movement variables from video pose estimation constrain decision parameters on a trial-by-trial basis. We find the mDDM provides a better model fit to rats' decisions in the free response accumulation task than traditional DDM models. Interestingly, on each trial we observed a period of time, prior to choice, that was characterized by head immobility. The length of this period was positively correlated with the rats' decision bounds and stimuli presented during this period had the greatest impact on choice. Together these results support a model in which internal decision dynamics are reflected in movements and demonstrate that inclusion of movement parameters improves the performance of diffusion-to-bound decision models.

A computational account of conflict processing during mental imagery.

Previous studies examining conflict processing within the context of a color-word Stroop task have focused on both stimulus and response conflicts. However, it has been unclear whether conflict can emerge independently of stimulus conflict. In this study, a novel arrow-gaze mental-rotation Stroop task was introduced to explore the interplay between conflict processing and mental rotation. A modelling approach was utilized to provide a process-level account of the findings. The results of our Stroop task indicate that conflict can emerge from mental rotation in the absence of stimulus conflict. The strength of this imagery conflict effect decreases and even reverses as mental rotation angles increase. Additionally, it was observed that participants responded more quickly and with greater accuracy to small rather than large face orientations. A comparison of three conflict diffusion models-the diffusion model for conflict tasks (DMC), the dual-stage two-phase model (DSTP), and the shrinking spotlight model (SSP)-yielded consistent support for the DSTP over the DMC and SSP in the majority of instances. The DSTP account of the experimental results revealed an increased nondecision time with increasing mental rotation, a reduction in interference from incompatible stimuli, and an improved drift rate in response selection phase, which suggests enhanced cognitive control. The findings from the model-based analysis provide evidence for a novel interaction between cognitive control and mental rotation.

Physically stressed bees expect less reward in an active choice judgement bias test.

Emotion-like states in animals are commonly assessed using judgment bias tests that measure judgements of ambiguous cues. Some studies have used these tests to argue for emotion-like states in insects. However, most of these results could have other explanations, including changes in motivation and attention. To control for these explanations, we developed a novel judgment bias test, requiring bumblebees to make an active choice indicating their interpretation of ambiguous stimuli. Bumblebees were trained to associate high or low rewards, in two different reward chambers, with distinct colours. We subsequently presented bees with ambiguous colours between the two learnt colours. In response, physically stressed bees were less likely than control bees to enter the reward chamber associated with high reward. Signal detection and drift diffusion models showed that stressed bees were more likely to choose low reward locations in response to ambiguous cues. The signal detection model further showed that the behaviour of stressed bees was explained by a reduction in the estimated probability of high rewards. We thus provide strong evidence for judgement biases in bees and suggest that their stress-induced behaviour is explained by reduced expectation of higher rewards, as expected for a pessimistic judgement bias.

Manipulating Prior Beliefs Causally Induces Under- and Overconfidence.

Humans differ vastly in the confidence they assign to decisions. Although such under- and overconfidence relate to fundamental life outcomes, a computational account specifying the underlying mechanisms is currently lacking. We propose that prior beliefs in the ability to perform a task explain confidence differences across participants and tasks, despite similar performance. In two perceptual decision-making experiments, we show that manipulating prior beliefs about performance during training causally influences confidence in healthy adults (N = 50 each; Experiment 1: 8 men, one nonbinary; Experiment 2: 5 men) during a test phase, despite unaffected objective performance. This is true when prior beliefs are induced via manipulated comparative feedback and via manipulated training-phase difficulty. Our results were accounted for within an accumulation-to-bound model, explicitly modeling prior beliefs on the basis of earlier task exposure. Decision confidence is quantified as the probability of being correct conditional on prior beliefs, causing under- or overconfidence. We provide a fundamental mechanistic insight into the computations underlying under- and overconfidence.

Teleological reasoning bias is predicted by pupil dynamics: Evidence for the extensive integration account of bias in reasoning.

Teleological reasoning is the tendency for humans to see purpose and intentionality in natural phenomena when there is none. In this study, we assess three competing theories on how bias in reasoning arises by examining performance on a teleological reasoning task while measuring pupil size and response times. We replicate that humans (N = 45) are prone to accept false teleological explanations. Further, we show that errors on the teleological reasoning task are associated with slower response times, smaller baseline pupil size, and larger pupil dilations. The results are in line with the single-process extensive integration account and directly oppose predictions from dual-processing accounts. Lastly, by modeling responses with a drift-diffusion model, we find that larger baseline pupil size is associated with lower decision threshold and higher drift rate, whereas larger pupil dilations are associated with higher decision threshold and lower drift rate. The results highlight the role of neural gain and the Locus Coeruleus-Norepinephrine system in modulating evidence integration and bias in reasoning. Thus, teleological reasoning and susceptibility to bias likely arise due to extensive processing rather than through fast and effortless processing.

Attention facilitates initiation of perceptual decision making: a combined psychophysical and electroencephalography study.

Humans can selectively process information and make decisions by directing their attention to desired locations in their daily lives. Numerous studies have shown that attention increases the rate of correct responses and shortens reaction time, and it has been hypothesized that this phenomenon is caused by an increase in sensitivity of the sensory signals to which attention is directed. The present study employed psychophysical methods and electroencephalography (EEG) to test the hypothesis that attention accelerates the onset of information accumulation. Participants were asked to discriminate the motion direction of one of two random dot kinematograms presented on the left and right sides of the visual field, one of which was cued by an arrow in 80% of the trials. The drift-diffusion model was applied to the percentage of correct responses and reaction times in the attended and unattended fields of view. Attention primarily increased sensory sensitivity and shortened the time unrelated to decision making. Next, we measured centroparietal positivity (CPP), an EEG measure associated with decision making, and found that CPP latency was shorter in attended trials than in unattended trials. These results suggest that attention not only increases sensory sensitivity but also accelerates the initiation of decision making.

Cognitive deficits and enhancements in youth from adverse conditions: An integrative assessment using Drift Diffusion Modeling in the ABCD study.

Childhood adversity can lead to cognitive deficits or enhancements, depending on many factors. Though progress has been made, two challenges prevent us from integrating and better understanding these patterns. First, studies commonly use and interpret raw performance differences, such as response times, which conflate different stages of cognitive processing. Second, most studies either isolate or aggregate abilities, obscuring the degree to which individual differences reflect task-general (shared) or task-specific (unique) processes. We addressed these challenges using Drift Diffusion Modeling (DDM) and structural equation modeling (SEM). Leveraging a large, representative sample of 9-10 year-olds from the Adolescent Brain Cognitive Development (ABCD) study, we examined how two forms of adversity-material deprivation and household threat-were associated with performance on tasks measuring processing speed, inhibition, attention shifting, and mental rotation. Using DDM, we decomposed performance on each task into three distinct stages of processing: speed of information uptake, response caution, and stimulus encoding/response execution. Using SEM, we isolated task-general and task-specific variances in each processing stage and estimated their associations with the two forms of adversity. Youth with more exposure to household threat (but not material deprivation) showed slower task-general processing speed, but showed intact task-specific abilities. In addition, youth with more exposure to household threat tended to respond more cautiously in general. These findings suggest that traditional assessments might overestimate the extent to which childhood adversity reduces specific abilities. By combining DDM and SEM approaches, we can develop a more nuanced understanding of how adversity affects different aspects of youth's cognitive performance. RESEARCH HIGHLIGHT: To understand how childhood adversity shapes cognitive abilities, the field needs analytical approaches that can jointly document and explain patterns of lowered and enhanced performance. Using Drift Diffusion Modeling and Structural Equation Modeling, we analyzed associations between adversity and processing speed, inhibition, attention shifting, and mental rotation. Household threat, but not material deprivation, was mostly associated with slower task-general processing speed and more response caution. In contrast, task-specific abilities were largely intact. Researchers might overestimate the impact of childhood adversity on specific abilities and underestimate the impact on general processing speed and response caution using traditional measures.

Orienting to fear under transient focal disruption of the human amygdala.

Responding to threat is under strong survival pressure, promoting the evolution of systems highly optimized for the task. Though the amygdala is implicated in 'detecting' threat, its role in the action that immediately follows-'orienting'-remains unclear. Critical to mounting a targeted response, such early action requires speed, accuracy, and resilience optimally achieved through conserved, parsimonious, dedicated systems, insured against neural loss by a parallelized functional organization. These characteristics tend to conceal the underlying substrate not only from correlative methods but also from focal disruption over time scales long enough for compensatory adaptation to take place. In a study of six patients with intracranial electrodes temporarily implanted for the clinical evaluation of focal epilepsy, we investigated gaze orienting to fear during focal, transient, unilateral direct electrical disruption of the amygdala. We showed that the amygdala is necessary for rapid gaze shifts towards faces presented in the contralateral hemifield regardless of their emotional expression, establishing its functional lateralization. Behaviourally dissociating the location of presented fear from the direction of the response, we implicated the amygdala not only in detecting contralateral faces, but also in automatically orienting specifically towards fearful ones. This salience-specific role was demonstrated within a drift-diffusion model of action to manifest as an orientation bias towards the location of potential threat. Pixel-wise analysis of target facial morphology revealed scleral exposure as its primary driver, and induced gamma oscillations-obtained from intracranial local field potentials-as its time-locked electrophysiological correlate. The amygdala is here reconceptualized as a functionally lateralized instrument of early action, reconciling previous conflicting accounts confined to detection, and revealing a neural organisation analogous to the superior colliculus, with which it is phylogenetically kin. Greater clarity on its role has the potential to guide therapeutic resection, still frequently complicated by impairments of cognition and behaviour related to threat, and inform novel focal stimulation techniques for the management of neuropsychiatric conditions.

Midfrontal theta phase underlies evidence accumulation and response thresholding in cognitive control.

Cognitive control involves evidence accumulation and response thresholding, but the neural underpinnings of these 2 processes are poorly understood. Based on recent findings that midfrontal theta phase coordinates the correlation between theta power and reaction time during cognitive control, this study investigated whether and how theta phase would modulate the relationships between theta power and evidence accumulation and response thresholding in human participants when they performed a flanker task. Our results confirmed the modulation of theta phase on the correlations between ongoing midfrontal theta power and reaction time under both conditions. Using hierarchical drift-diffusion regression modeling, we found that in both conditions, theta power was positively associated with boundary separation in phase bins with optimal power-reaction time correlations, whereas the power-boundary correlation decreased to nonsignificance in phase bins with reduced power-reaction time correlations. In contrast, the power-drift rate correlation was not modulated by theta phase, but by cognitive conflict. Drift rate was positively correlated with theta power for the bottom-up processing in the non-conflict condition, whereas it was negatively correlated with theta power for the top-down control to address conflict. These findings suggest that evidence accumulation is likely to be a phase-coordinated continuous process, whereas thresholding may be a phase-specific transient process.